(Crustacea: Decapoda) at Bear Cut, Biscayne Bay, Florida, Usa

BULLETIN OF MARINE SCIENCE, 67(2): 773–788, 2000

DIVERSITY AND RECRUITMENT OF PENAEOID SHRIMPS (CRUSTACEA: DECAPODA) AT BEAR CUT, BISCAYNE BAY, FLORIDA, USA

Maria M. Criales, Maria J. Bello and Cynthia Yeung

ABSTRACT Postlarval and juvenile penaeoid shrimps were collected with moored channel nets at Bear Cut, a tidal pass between the Atlantic and Biscayne Bay, Florida, from January through December 1994. Results show a much higher number of species than in previous reports. Among juveniles, Metapenaeopsis spp., which comprised five species, was the most abundant and diverse genus. Two of them, M. martinella and M. hobbsi, constitute new records for North American waters. Despite the abundance of Metapenaeopsis spp., neither small juveniles (CL <2.0 mm) nor larger adults (CL >12.5 mm) were caught at Bear Cut. The genus Farfantepenaeus was represented by the pink shrimp, F. duorarum, and the pink spotted shrimp, F. brasiliensis, in a proportion of 2:1. Monthly mean densities of the juvenile penaeoids Farfantepenaeus spp., Metapenaeopsis spp., Sicyonia spp., and Rimapenaeus constrictus showed a seasonal pattern. Densities were lowest between May and October, and highest between December and February. A two-factor repeated- measures ANOVA of density by depth and tidal period showed that depth does not have a significant effect on the density for any of the juvenile taxa, but the effect of the tidal period is highly significant (α = 0.05). The reverse result was obtained for Farfantepenaeus spp. postlarvae; depth effect was significant but not tidal period. F. duorarum and F. brasiliensis juveniles exhibited the greatest carapace length in January and February, when the highest density of shrimps were leaving the Bay. Farfantepenaeus spp. postlarvae showed a bimodal distribution with peaks in March and November.

Biscayne Bay shelters a great diversity of species of fishes and invertebrates. Over 152 species of decapods have been identified by Voss et al. (1969). This diversity is the result of an extensive coastline with varied marine and estuarine habitats (mangrove forests, coral reefs and seagrasses) and the juncture of the northern Carolinian and Caribbean biogeographic regions. The Florida Current, which brings larvae from upstream sources in the Caribbean Sea and the Gulf of Mexico, runs very close to shore (Lee et al., 1992). Biscayne Bay is an important nursery ground for penaeid shrimp (Berkeley et al., 1985; McKinley, 1995). A small but valuable live bait shrimp fishery has operated in Biscayne Bay since at least the early 1950s, supporting a continually growing recreational fishing industry (Berkeley et al., 1985; Iversen et al., 1993). In 1993 the estimated total commercial bait shrimp harvest from Biscayne Bay had a retail value of $1.7 million (Coleman et al., 1993). The pink shrimp Farfantepenaeus duorarum is by far the most important species supporting the live bait shrimp fishery in Biscayne Bay, and the pink spotted shrimp Farfantepenaeus brasiliensis has been reported as part of the fishery (Iversen and Van Meter, 1964; Saloman et al., 1968; Berkeley and Campos, 1984). In addition to Farfantepenaeus spp. seven other penaeoid species have been reported from Biscayne Bay in taxonomic reviews, but none of these works provide quantitative data on these species (Voss et al., 1969; Pérez Farfante, 1970, 1971b; Berkeley and Campos, 1984; Biosystems Research, Inc. 1984).

773 774 BULLETIN OF MARINE SCIENCE, VOL. 67, NO. 2, 2000

Although the recruitment of juvenile pink shrimp in the Everglades National Park in Florida Bay is relatively well understood (e.g., Tabb et al., 1962; Costello et al., 1986; Yokel et al., 1969; Sheridan, 1996), the origin of the juvenile pink shrimp population recruiting in Biscayne Bay is unclear. It has been assumed that the pink shrimp that recruit to Biscayne Bay belong to the Dry Tortugas population off southwest Florida. F. duorarum females from the Tortugas grounds spawn all year round. The highest frequency of ripe females (e.g., Cummings, 1961) and the highest peaks of larval abundance (Jones et al., 1970; Munro et al., 1968) occur between April and July. Research on the spatio- temporal variability of early development stages of pink shrimp in the Dry Tortugas area and their relation with small- and mesoscale structures of the Florida Current has shown that there are at least two basic transport mechanisms for postlarvae in the Tortugas area. Pink shrimp larvae may migrate from where they were spawned in the Dry Tortugas via the Florida Current and then back into Florida Bay through passes in the middle Keys (Munro et al., 1968; Jones et al., 1970). Other postlarvae may be retained at the spawning area by the cyclonic circulation of the Tortugas Gyre, followed by movements to the southwest Florida shelf and Florida Bay by winds and tidal currents (Criales and Lee, 1995). For Biscayne Bay the only information about juvenile penaeids comes from the bait fishery (Berkeley and Campos, 1984; Berkeley et al., 1985; McKinley, 1995; Ault et al., 1999). Research on abundance and seasonality of postlarvae in Biscayne Bay has not been undertaken. This research was conducted to describe the patterns of movement and abundance of penaeoid postlarvae into Biscayne Bay through Bear Cut, the emigration of penaeoid juvenile shrimp from the Bay, and to discuss possible larval origins and juvenile fates. This research formed part of the Southeast Florida Caribbean and Recruitment Project (SEFCAR) of the University of Miami’s Rosenstiel School of Marine and Atmospheric Science (RSMAS/UM) and the National Oceanographic and Atmospheric Administra- tion (NOAA).

MATERIAL AND METHODS

Biscayne Bay is a shallow subtropical lagoon located on the southeast coast of Florida. Approxi- mately 90 km long, the Bay is connected with continental shelf waters through a complicated net- work of tidal inlets. Bear Cut is one of those tidal inlets (approximately 570 m wide and 4.6 m deep) located between Key Biscayne and Virginia Key (Fig. 1). Water moving through Bear Cut strongly influences the circulation in the central part of the Bay (Lee, 1975).Tides in Biscayne Bay are semidiurnal and the amplitude ranges from 30 to 60 cm, with a period of 12.4 h (Van De Kreeke, 1976). Since Biscayne Bay is shallow, there is virtually no stratification of the water column and the water is readily mixed by wind events (Lee, 1975; Johnson and Lee, 1977). Sampling was conducted at Bear Cut during the new moon periods of January through Decem- ber 1994 by E. Maddox (RSMAS/UM, unpubl.). Two moored channel nets were used to sample settlement and juvenile stages of fishes and shrimps at a single station (Table 1). Nets (2 mm mesh) swing freely with tidal changes. A surface net with a mouth area 2 m wide × 1 m deep (2 m2) was suspended between 0 and 1 m in depth, and a subsurface net with a mouth area 2 m wide × 2 m deep (4 m2) was suspended between 1 and 3 m deep. Sampling during each new moon took place on four consecutive days in which samples were collected during flood and mixed ebb-flood tides. For the flood-tide samples, nets were set for about 6 h at night, from the slack tide around sunset until around midnight. For the mixed tide samples, nets were set for about 12 h including 6 h of darkness, from the high slack tide at midnight until the next high slack occurring the next morning. General CRIALES ET AL.: PENAEOID SHRIMPS IN BISCAYNE BAY, FLORIDA 775

Figure 1. Location of the study site (•) at Bear Cut, Biscayne Bay on the southeast coast of Florida, USA.

Oceanic flowmeters were mounted in the mouth of each net. Samples were washed and fixed in ethanol. Postlarvae and juvenile penaeoid shrimps were sorted and identified to genera and species (Dobkin, 1961; Cook, 1966; Williams, 1965,1984; Abele and Kim, 1986; Pérez Farfante, 1969,1970, 1971a, 1971b, 1980, 1988; Chuensri, 1968; Chace, 1972). Scientific names of genera and species follow those proposed in the most recent taxonomical review of the penaeoid shrimps (Pérez Farfante and Kensley, 1997). Among the most relevant taxonomic changes are the raising of Penaeus subgenera to generic level (e.g., Penaeus (Farfantepenaeus) duorarum = Farfantepenaeus duorarum) and the segregation of the genus Rimapenaeus from Trachypenaeus s.l. Total length (TL, from tip of ros- trum to tip of telson) and carapace length (CL, from postorbital margin to mid-dorsal posterior margin of the carapace) were measured for juvenile shrimps and for 10 randomly chosen postlarvae per sample. Postlarvae were separated by development stages according to the number of rostral dorsal spines (Ewald, 1965). A group of small juvenile Farfantepenaeus spp. with CL <12 mm were not identifiable to species because the thelyca and petasmata were not completely developed. The raw catch in each sample was standardized to the density per 1000 m3 of sea water filtered. A two-factor repeated-measures ANOVA design was used to test the effects of (1) depth strata (surface and subsurface) and (2) repeated measures of tidal periods (flood and mixed) within each depth stratum. Densities were tested for normality and homogeneity of variance, and most failing that (Bartlett χ2, P < 0.05), were all ln(x+1)-transformed (Bartlett χ2, P > 0.1) for the ANOVA. The mean density and the variance of shrimps caught over the 4 d of sampling of each month were calculated using the delta-lognormal method (Pennington, 1983), which assumes a lognormal distribution of the positive density observations. The mean and variance estimates were constructed as the product of the proportions of samples with positive density and the average density for those positive samples, and 95% lognormal confidence intervals were associated with the means. The 776 BULLETIN OF MARINE SCIENCE, VOL. 67, NO. 2, 2000

Table 1. Summary of sampling at Bear Cut, Biscayne Bay, Florida, during 1994.

Date Total number of Surface/subsurface Flood/mixed Total raw catch of 1994 samples samples flood+ebb samples penaeoid shrimps 1/9−15/13 1877/ 89/ 35 2/8−20/12 20100/1 130/1 44 3/10−34/14 1778/ 62/ 14 4/9−40/13 20100/1 100/1 14 5/8−50/12 20100/1 100/1 3 6/7−68/11 1999/ 90/ 5 7/6−70/10 20100/1 180/1 2 8/5−80/9 20100/1 150/1 9 9/3−92/9 21121/1 190/1 8 10/3−100/7 20100/1 110/1 6 11/1−101/5 20100/1 150/1 91 11/30−102/4 20100/1 130/1 20

monthly pattern of density of each taxon was examined with possible environmental correlates. Water temperature, tidal phase, and wind speed and direction data were collected at Virginia Key, National Oceanographic Service Tide Station NOAA/ NOS/ NGWLS located at Bear Cut. Precipi- tation data were obtain from the NOAA Local Climatological Data (NOAA, 1994).

RESULTS

DIVERSITY AND ABUNDANCE.—A total of 1528 juvenile penaeoid shrimps and 1020 Farfantepenaeus spp. postlarvae were collected at Bear Cut during January–December, 1994. Eleven species of penaeoids were identified (Fig. 2A–D). The family Penaeidae comprised the grooved shrimps pink shrimp F. duorarum (Burkenroad, 1939) and pink spotted shrimp F. brasiliensis (Latrille, 1817); Caribbean velvet shrimp Metapenaeopsis goodei (Smith, 1885) and four other velvet shrimp species, M. martinella (Pérez Farfante, 1971a), M. hobbsi (Pérez Farfante, 1971a), M. smithi (Schmitt, 1924) and M. gerardoi (Pérez Farfante, 1971a); and the roughneck shrimp Rimapenaeus constrictus (Stimpson, 1874). The Family Sicyoniidae comprised kinglet rock shrimp, Sicyonia typica (Boeck, 1864) and two other rock shrimp species, S. laevigata (Stimpson, 1871) and S. parri (Burkenroad, 1934). Farfantepenaeus was represented by postlarval and juvenile stages, while the other three genera were only represented by juveniles (Fig. 2A). Overall, Metapenaeopsis spp. juveniles comprised the highest percentage (34.2%) of the total catch of juveniles and postlarvae, followed by Farfantepenaeus spp. postlarvae (32.4%) and Farfantepenaeus spp. juveniles (27.8%). Among juveniles alone, Metapenaeopsis spp. made up the highest percentage (50.6%), followed by Farfantepenaeus (41.2%). The Caribbean velvet shrimp M. goodei was the most abundant species identified (catch per 1000 m3 = 418) (Fig. 2B). F. duorarum made up 75% and F. brasiliensis 25% of the identified Farfantepenaeus spp. (Fig. 2C). Sicyoniid rock shrimps were scarce (6.3% of the total catch) with S. typica making 70% of the rock shrimp species (Fig. 2D). A few juveniles of the roughneck shrimp R. contrictus were captured at Bear Cut (1.7% of the total catch). In addition to being very abundant, Metapenaeopsis spp. were also the most diverse at Bear Cut (Fig. 2B). The five Metapenaeopsis species that have been recorded from the CRIALES ET AL.: PENAEOID SHRIMPS IN BISCAYNE BAY, FLORIDA 777

Figure 2. (A) Relative percentages of the standardized density (shrimp/1000 m3) of penaeoid shrimps at Bear Cut, Biscayne Bay, Florida, January–December, 1994. A Postlarvae and juvenile shrimps grouped by genera. (B) Velvet shrimp species (Metapenaeopsis spp.). (C) Pink shrimp and pink spotted shrimp (Farfantepenaeus spp.). (D) Rock shrimp species (Sicyonia spp.). 778 BULLETIN OF MARINE SCIENCE, VOL. 67, NO. 2, 2000

western Atlantic (Pérez Farfante, 1971a) were found at Bear Cut; thus this constitutes the first report of all five Metapenaeopsis species in a single geographical area. M. martinella and M. hobbsi are recorded here for the first time in North American waters. Records of M. martinella were previously restricted to the Caribbean and the Atlantic coast of South America, and those of M. hobbsi to the Bahamas, Antilles, Caribbean and South America (Pérez Farfante, 1971a; Abele and Kim, 1986). M. goodei and M. martinella were the two most abundant Metapenaeopsis species found at Bear Cut, making up 15.9% and 12.8% of the total catch respectively. Despite the high density of juvenile Metapenaeopsis spp., neither postlarvae nor mature individuals were caught at Bear Cut. SEASONALITY.—Water temperature during the days of sampling and monthly precipitation displayed a seasonal cycle typical of the southeastern USA (Fig. 3A). Maximum water temperatures of around 30oC occurred in the summer months of July to September, dropping to a minimum of around 22oC in the winter month of January. Total monthly precipitation also peaked in summer with 43 cm in August and 34 cm in September, but all the preceding months from January to July were relatively dry with only 5–15 cm of precipitation monthly. The monthly mean densities of the juveniles of Farfantepenaeus spp., Metapenaeopsis spp., Sicyonia spp. and R. constrictus showed a marked seasonal pattern (Fig. 3B–F). Densities for the juveniles of all taxa were generally lowest between May–October, and highest between December–February. The monthly mean density distribution patterns are highly significantly correlated among the juveniles of all taxa but not for postlarvae (Spearman is r, P < 0.001, Table 2) and especially between juveniles of Farfantepenaeus spp. and Metapenaeopsis spp. (Spearman r = 0.8983, P <.0001). Juvenile density patterns of all taxa were distinctly different from that of Farfantepenaeus spp. postlarvae (Table 2), which seemed to be bimodal with peaks in March and November (Fig. 3F). DEPTH AND TIDE.—The depth of the net did not have a significant effect on the density for any of the juvenile taxa, but the effect of the tidal period was highly significant (α = 0.05, Table 3). The reverse was true for Farfantepenaeus spp. postlarvae–depth effect was significant but not tidal period. A significantly higher density of Farfantepenaeus spp. postlarvae was found in the subsurface than in the surface net. The monthly mean density (subsurface and surface nets combined) patterns by tidal period (flood, mixed) for each taxon are shown in Figure 3B–F. The juveniles of all taxa were more concentrated in the mixed-tide samples than in the flood-tide samples. R. constrictus in particular did not appear at all in flood-tide samples. The reverse pattern was seen in Farfantepenaeus spp. postlarvae, which were more concentrated in the flood-tide samples. SIZE OF POSTLARVE AND JUVENILES.—The size of Farfantepenaeus spp. postlarvae ranged from 1.5–3.7 mm CL (Fig. 4A) and the highest percentage frequency fell in the size class of 2.0–2.4 mm CL. The number of rostral spines of postlarvae ranged from 2 to 5 with a mode of 4 (62%). The estimated age of postlarvae of this size and number of rostral spines is 25 d (Ewald, 1965). The monthly mean CL of postlarvae was relatively higher from January to May than from October to December (Fig. 4B). The highest frequency of Farfantepenaeus spp. juveniles falls in the size class of 6-–10 mm CL (Fig. 4C). Percentages fell progressively with increasing size classes. The lowest percentages of juveniles are <6 mm and >26 mm CL. Monthly mean CL of F. brasiliensis (n = 125, grand mean ± SD = 17.7 ± 5.2 mm) were larger than those of F. duorarum (n = 258, grand mean ± SD = 15.1 ± 4.0 mm) in each month except November (Fig. 4D). The maximum CL recorded for F. brasiliensis was 34.0 mm, while that of F. duorarum was CRIALES ET AL.: PENAEOID SHRIMPS IN BISCAYNE BAY, FLORIDA 779

Figure 3. (A) Monthly mean water temperature (oC) and total precipitation (cm) recorded at Virginia Key during 1994. B–F) Monthly mean densities (combining surface and subsurface catch and standardized to per 1000 m3 of seawater filtered) by tidal period (flood, mixed) of juveniles of Metapenaeopsis spp., Farfantepenaeus spp., Sicyonia spp, and Rimapenaeus constrictus, and postlarvae of Farfantepenaeus spp. Means were estimated using the delta-lognormal method and error bars represent 95% lognormal confidence intervals about means. 780 BULLETIN OF MARINE SCIENCE, VOL. 67, NO. 2, 2000

Table 2. Spearman paired correlations (r) and the levels of significance (P) among the monthly mean densities of taxa caught at Bear Cut in 1994. Bold face indicates significant effects.

Rimapenaeus Sicyonia spp. Farfantepenaeus spp. Farfantepenaeus spp. constrictus postlarvae juveniles Sicyonia spp. 0.2844 P = 0.0004 Farfantepenaeus −0.0066 0.0431 sPpp. postlarvae = 0P.9216 = 0.5183 Farfantepenaeus 03.2476 0.587 0.0487 spp. juveniles P = 0P.0007 = 0.0000 P = 0.4658 Metapenaeopsis spp. 03.259 0.548 0.0575 0.8983 P = 0P.0009 = 0.0000 P = 0.3897 P = 0.0000

24.5 mm. The highest mean CL occurred in January for F. duorarum (CL = 17.5 ± 3.7 mm) and in February for F. brasiliensis (CL = 21.5 ± 4.7 mm). These values correspond with data of the bait shrimp fishery from Biscayne Bay (Berkeley et al., 1985; McKinley, 1995), indicating that the highest densities of juveniles leave the Bay in January and February (Fig. 3C). Carapace lengths of these species decreased to a minimum in May (F. duorarum, CL = 9.5 mm; F. brasiliensis, CL = 11.5 mm) coinciding with the minimal density of shrimps during the entire year. Neither small juveniles (CL <4.0 mm) nor larger adults (CL >12.5 mm) of Metapenaeopsis spp. were caught at Bear Cut (Fig. 4E). The percentage frequency of Metapenaeopsis spp. juveniles shows a mode in the size class of 8–9.9 mm. Size frequency distributions of M. goodei and M. martinella fall in a normal distribution (Chi- square test, for M. goodei χ2 = 4.14 ×10−5, P < 0.001, for M. martinella χ2 = 4.6 × 10−6, P < 0.001). Monthly averages of CL for the velvet shrimps M. goodei and M. martinella showed similar patterns with no significant differences among months and no significant size differences between species (Fig. 4F). Mean CL of females was higher than that of males for both species (M. goodei females CL = 7.52 ± 1.8 mm, males CL = 7.43 ± 1.2 mm; M. martinella females CL = 7.3 ± 2 mm, males CL = 6.4 ± 1.9 mm).

DISCUSSION

Biscayne Bay grooved juvenile shrimps typically have been treated as one population (Berkeley, et al., 1985; McKinley, 1995; Ault et al., 1999), in large part because Farfantepenaeus species are so close in both meristic and morphometric characters (Pérez Farfante, 1970). Eldred (1960) and Iversen and Van Meter (1964) reported that a few F. brasiliensis co-occurred with F. duorarum in Biscayne Bay. Saloman et al. (1968) also identified in Biscayne Bay three Farfantepenaeus species: pink shrimp F. duorarum was the most abundant (86.4%) of all Farfantepenaeus and was present every month; spotted pink shrimp F. brasiliensis (13.6% of the total) was captured in greatest numbers in June– October; and brown shrimp F. aztecus was represented by a single specimen. In this study F. brasiliensis showed a much higher frequency of occurrence and a different seasonal pattern from previous reports. F. brasiliensis made up 25% of the identified Farfantepenaeus spp., being present every month of the year with its maximum peak of abundance in January and a small peak in April. Specimens of the brown shrimp F. aztecus CRIALES ET AL.: PENAEOID SHRIMPS IN BISCAYNE BAY, FLORIDA 781

Figure 4. Size frequency distribution of carapace length and the monthly average of carapace length (mm) standard deviation for shrimps captured at Bear Cut, Biscayne Bay, Florida, January–December, 1994. (A–B) Farfantepenaeus spp. postlarvae, (C–D) Farfantepenaeus duorarum and F. brasiliensis juveniles. (E–F) Metapenaeopsis goodei and M. martinella juveniles. 782 BULLETIN OF MARINE SCIENCE, VOL. 67, NO. 2, 2000

Table 3. Two-factor ANOVA testing for differences in the density (ln(n+1)−transformed, where n is the catch/1000 m3) due to the (1) depth of sampling (surface or subsurface) in repeated measurements over the (2) tidal period (flood or mixed). Bold face indicates significant effects.

Efffect dSMfdSMFP etffect erffec errro erro

Metapenaeopsis d14epth 05.242 150 06.825 00.293 0.589 spp. juveniles t12ide 457.211 180 06.631 704.729 0.000 d18epth*tide 05.001 180 08.631 01.002 0.958

Farfantepeneaus d16epth 15.217 190 08.796 12.527 0.219 spp. juveniles t19ide 756.686 100 04.792 906.823 0.000 d10epth*tide 05.110 100 08.792 02.138 0.710

Sicyonia d17epth 05.147 110 09.475 03.310 0.578 spp. juveniles t16ide 65.536 120 09.282 203.159 0.000 d10epth*tide 05.122 120 02.282 04.432 0.512

Rimapenaeus d14epth 05.243 180 03.151 12.603 0.208 constrictus juveniles t15ide 25.428 180 08.151 115.995 0.000 d14epth*tide 05.243 180 03.151 12.603 0.208

Farfantepeneaus d15epth 25.610 180 09.607 47.294 0.040 sepp. postlarvae t14id 05.517 140 02.484 17.068 0.303 d19epth*tide 05.119 140 06.484 08.247 0.619

were not found at Bear Cut. The difference in species composition and temporal patterns found between the present research and the previously mentioned works might be due to difficulties in the identification of Farfantepenaeus species or a shift in species composition in the past two decades. Location of sampling and different gear types should not be major factors in the different research results. Bear Cut has been a sampling station in previous studies (Berkeley, et al., 1985; McKinley, 1995; Ault et al., 1999). The channel nets used in the present study collect smaller size classes of shrimps than trawl nets, which were used in previous research. However F. brasiliensis shrimps are larger than F. duorarum. The origin of F. brasiliensis recruiting in Biscayne Bay is unclear. Spawning grounds of F. brasiliensis have not been identified in waters off the southeast or southwest coast of Florida (Iversen et al., 1993). The only known penaeid spawning grounds in the area are the Tortugas grounds, where the penaeid population is considered to consist almost ex- clusively of F. duorarum (Costello and Allen, 1970). It is very rare to find even a single F. brasiliensis in samples from the Tortugas (Pérez Farfante, 1969; Pérez Farfante, pers. com.). F. brasiliensis is the dominant species of the shrimp fishery in the Bahamas, Cuba and Quintana Roo, Mexico (Pérez Farfante, 1969). However, no research has been undertaken to determine if F. brasiliensis larvae come from distant regions or if it is a locally recruited population. Larval transport from the Gulf of Mexico via the Loop Current to the Florida Keys has recently been shown for the slipper lobster Scyllarides nodifer and the sand crab Albunea sp. (Yeung, 1996; Yeung et al., in press). This pathway, which is CRIALES ET AL.: PENAEOID SHRIMPS IN BISCAYNE BAY, FLORIDA 783 associated with the timing and combination of the latitudinal position of the Loop Cur- rent and the northeast Gulf of Mexico outflow, could be responsible for intrusions of larvae from the Gulf of Mexico and the Caribbean into the west and east coast of Florida. The largest number of penaeoid juveniles was caught during the winter months. F. duorarum and F. brasiliensis showed the highest abundance and largest sizes in January. These data corroborated the bait shrimp fishery data from Biscayne Bay, which indicated that the greatest size and abundance of pink shrimp occurs in January (Berkeley et al., 1985, McKinley, 1995). It has not been determined whether juveniles emigrating from Biscayne Bay recruit into the Tortugas Grounds or migrate further north via the Florida Current to the fishery grounds off northeast Florida. This winter emigration of juvenile pink shrimp from Biscayne Bay does not follow the emigration patterns from other Florida nursery grounds. Emigration from nursery areas in Everglades National Park is year- round with early spring and late summer peaks (Tabb et al., 1962; Yokel et al., 1969; Costello et al., 1986; Sheridan, 1996). Emigration of juvenile pink shrimp from the nursery grounds of Florida Bay in summer and fall has been postulated to form the fall and winter landings of new recruits to the Tortugas Grounds (Higman et al., 1972). Similar fall and spring emigrations of juvenile pink shrimp occur from Tampa Bay, northwest coast and from northeast Florida estuaries between Daytona Beach and Cape Canaveral (Eldred et al., 1961; Huff and Cobb, 1979; Kennedy and Barber, 1981). The mechanisms that penaeid postlarvae use to approach and enter estuaries seem to be highly variable depending on the species and the environmental stimuli (Heron et al., 1994). Farfantepenaeus postlarvae entering Biscayne Bay through Bear Cut were found to be highly abundant in the subsurface layer during flood tide. Pink shrimp postlarvae nearshore may use tidal currents in combination with vertical migration to advance to- wards the coast. There is solid evidence that this mechanism is used by Penaeus merguiensis postlarvae in the Gulf of Carpentaria, Australia, to advect along the coast up to 160 km over a 20 d period (Rothlisberg et al., 1985; Staples and Vance, 1985). However, tidal currents were not a means of cross-shelf advection for Penaeus plebejus on the open shelf of southeastern Australia (Rothlisberg and Church, 1994). Hughes (1969a,b) demonstrated in laboratory experiments that postlarval and juvenile pink shrimp reacted to changes in salinity by changing swimming direction, and under certain circumstances, showed endogenous activity rhythms. Hughes (1969a,b) results have confounded interpretation because responses were highly variable and were not placed in a real ecological context. Furthermore, Biscayne Bay is a well-mixed estuary where there is not a sharp density gradient (Wang, 1986). Captures of Farfantepenaeus spp. and Metapenaeopsis spp. juveniles showed the highest densities in the surface stratum and during the ebb-flood mixed-tide periods. It seems that offshore emigration of juvenile penaeids near the surface on ebb tides is a common behavior pattern. Yokel (1969) sampled juvenile pink shrimp in Everglades National Park and found a consistently high proportion of juveniles migrating in the upper 50 cm of the channel during ebb tides. Staples and Vance (1986) reported massive emigration of juvenile P. merguiensis within 0.5 m of the water surface. Beardsley (1970) found similar results for F. duorarum and F. aztecus in Florida. Although penaeids could emigrate merely by using environmental cues, internal circadian and tidal rhythms could greatly assist the process (Dall et al., 1990, Garcia and Le Reste, 1981). Metapenaeopsis is the most speciose genus of the family Penaeidae and is represented in the Indo-Pacific by over 50 species, some of them of commercial significance (Crosnier, 784 BULLETIN OF MARINE SCIENCE, VOL. 67, NO. 2, 2000

1994 a,b; Dall et al., 1990). However, in the Western Atlantic, Metapenaeopsis is represented by only five species with very scattered distributions (Pérez Farfante, 1971a). All five species of the Western Atlantic were found at Bear Cut—the first report of all five Metapenaeopsis species in a single geographical area. M. goodei was previously recorded in Biscayne Bay (Voss et al.,1969; Pérez Farfante, 1970, 1971a; and Berkeley and Cam- pos, 1984). M. martinella and M. hobbsi are recorded here for the first time in North American waters. That M. martinella was the third most abundant species of penaeoid shrimps at Bear Cut indicates the limit of our knowledge of biodiversity in marine eco- systems. Despite the great abundance of Metapenaeopsis spp. juveniles, neither postlarvae nor mature individuals were caught at Bear Cut. There is no information available about life history, spawning grounds, or migrations for any of the Metapenaeopsis spp. from the western Atlantic. Metapenaeopsis spp. from the Indo-Pacific do not enter the estuaries, but they do migrate to coastal areas for protection (Dall et al., 1990). Metapenaeopsis spp. have been found in relatively small numbers in the interior of Biscayne Bay (Voss et al., 1969). The seasonal recruitment pattern found at Bear Cut may indicate that these species follow an annual cycle. In Mayaguez, Puerto Rico, M. goodei, M. martinella and M. smithi inhabiting the estuaries make up about 10% of the total abundance of penaeoid shrimps (Bauer, 1985). Metapenaeopsis juveniles from Puerto Rico showed a sharp in- crease in number from August to October. Juveniles of M. goodei, and M. martinella in Biscayne Bay showed the greatest abundance from December to April and reduced numbers from May to November.

ACKNOWLEDGMENTS

The authors gratefully acknowledge E. Maddox (RSMAS/UM) for sharing samples and data; I. Pérez Farfante (NOAA) for confirming identifications of shrimps; W. J. Richards (SFSC/ NOAA) for his continuous support; an anonymous reviewer for improving the text; N. Voss (RSMAS/UM) and the library personnel (RSMAS/UM) for logistic support; and all volunteers and students for their help in sampling and sorting.

LITERATURE CITED

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DATE SUBMITTED: December 9, 1999. DATE ACCEPTED: May 15, 2000.

ADDRESSES: (M.M.C.) Division of Marine Biology and Fisheries, Rosenstiel School of Marine and Atmospheric Science, University of Miami, 4600 Rickenbacker Causeway, Miami, Florida 33149. (M.J.B.) National Oceanographic and Atmospheric Administration, AOML, Miami, Florida 33149. (C.Y.) Cooperative Institute of Marine and Atmospheric Studies, Rosenstiel School of Marine and Atmospheric Science, University of Miami, 4600 Rickenbacker Causeway, Miami, Florida 33149. CORRESPONDING AUTHOR: (M.M.C.) Tel. 305-361-4073; E-mail: .