population structure of alpheus armillatus (decapoda, alpheidae)

JOURNAL OF CRUSTACEAN BIOLOGY, 26(1): 48–54, 2006

POPULATION STRUCTURE OF ALPHEUS ARMILLATUS (DECAPODA, ALPHEIDAE) IN ˜ O SEBASTIA ˜ O AND ILHABELA, SOUTHEASTERN BRAZIL SA E. C. Mossolin, R. M. Shimizu, and S. L. S. Bueno (ECM, corresponding author) (SLSB) Depto. de Zoologia (RMS) Depto. de Ecologia Instituto de Biocieˆncias, Universidade de Saõ Paulo, Rua do Mataõ # 101, Travessa 14 CEP 05508-900, Saõ Paulo, Brasil (ECM: [email protected]; SLSB: [email protected]; RMS: [email protected]) ABSTRACT The study of the population structure of A. armillatus was based on monthly collections (March 2000–February 2002) from two tidal flats— ´ gua Beach (EA), Ilhabela County—located at the northern portion of the Saõ Francisco Beach (SF), Saõ Sebastiaõ County, and Engenho d’A State of Saõ Paulo coast and separated by the 6 km wide Saõ Sebastiaõ Channel. Carapace length (CL) was measured to the nearest 0.01 mm. The proportion of ovigerous females and the embryonic development stage of eggs were recorded. The Von Bertalanffy growth equation was fit to modes of the temporal sequence of frequency distributions of CL classes (SF data). The same sampling effort yielded 547 males and 566 females at SF and 145 males and 150 females at EA. Proportions of ovigerous females were higher than 60% throughout the year in both sites. The temporal trend of percentage of late eggs indicated three annual hatching periods. Growth patterns of males and females were similar, with the former tending to grow more rapidly (K ¼ 2.28) and to attain smaller size (L‘ ¼ 13.90) than females (K ¼ 1.90; L‘ ¼ 14.90). The estimated longevity of males and females was 1.20 years (14.4 months) and 1.29 years (15.5 months), respectively.

INTRODUCTION

MATERIALS AND METHODS

Snapping shrimps of the family Alpheidae Rafinesque, 1815, are distributed worldwide and occur from the intertidal region to deep waters. Thirty-one genera are currently known (Holthuis, 1993) and six of those occur in Brazil (Christoffersen, 1998). Although several species of this family are commercially exploited in China, Japan, and Vietnam, they account for a small proportion of fisheries (Holthuis, 1980). According to the same author, only Alpheus heterochaelis Say, 1818, is exploited in small scale as fishing bait in Brazil. Studies on snapping shrimp populations are limited. They include description of reproductive cycle and interpretation of the secondary sexual characters of Synalpheus fritzmuelleri Coutie`re, 1909, and S. apioceros Coutie`re, 1909 (Felder, 1982); population dynamics of the sponge dwelling species S. brooksi Coutie`re, 1909, S. pectiniger Coutie`re, 1909, and S. longicarpus (Herrick, 1891) from the eastern Gulf of Mexico (Erdman and Blake, 1987); population structure of Alpheus dentipes Guerin, 1832, inhabiting calcareous algae in Spain (Fernańdez-Munõz and GarciaRaso, 1987); reproduction of species of the genus Alpheus Fabricius, 1798, from Puerto Rico (Bauer, 1989); and fecundity of sixteen species of Alpheidae from the United States (Corey and Reid, 1991). In Brazil, studies on Alpheidae are restricted to reports on occurrence of species in surveys on Decapoda (Quintino-Farias, 1980; Masunari et al., 1998), systematics and geographic distribution (Christoffersen, 1979, 1982), and observations on the association of Alpheus macrocheles (Hailstone, 1835) with calcareous algae (Ramos-Porto, 1979). The present study reports temporal population patterns of A. armillatus H. Milne Edwards, 1837, at two beaches located in the northern portion of the State of Saõ Paulo and includes information on sex ratio, larval release and recruitment periods, growth, and life span.

Fieldwork was conducted at two sites along the northern portion of the State of Saõ Paulo coast (Fig. 1): Saõ Francisco Beach (SF) (23844953.60S; 45824933.60W), Saõ Sebastiaõ County on the mainland and Engenho ´ gua Beach (EA) (23847944.60S; 45821956.90W), located on Saõ d’A Sebastiaõ Island, Ilhabela County. The two sites are 6 km apart, separated by the Saõ Sebastiaõ Channel. Both beaches presented a sandy slope on the higher portion of the intertidal zone, followed seaward by a flat with a substrate of a mixture of rocks and sediment of variable texture. At SF, the sediment was muddy and homogeneous all over the flat, while at EA gravels predominated and the muddy sediment was restricted to the upper half of the northern third of the flat. In addition, deposition of coarser gravel formed a distinct elevation (approximately 12 m long and 6 m wide) in the lower half of the central portion of the flat. Alpheus armillatus co-occurred with A. nuttingi (Schmitt, 1924) all over the intertidal flat at SF, showing no evident spatial segregation of species, although individuals of only one species, never both, were found under the same rock. At EA, A. armillatus was restricted to the muddy area of the flat while A. nuttingi occupied the predominant gravel sediment. An additional species, A. bouvieri A. Milne-Edwards, 1878, also occurred at EA, inhabiting the coarse gravel deposit. Sampling was conducted monthly from March 2000 to February 2002 during low tide periods in a 50 m long section in the central portion of the tidal flat of each site. Results of a preliminary survey showed that animals were abundant and all size classes were well represented in these areas. On each sampling date, water surface temperature and salinity were measured with a 0.18C scale thermometer and with a 1 ppt scale refractometer, respectively. Shrimps were collected manually from under the rocks of the exposed substrate. Very small specimens (carapace length , 4.5 mm) that did not present clear morphological differences were excluded from samples to avoid misidentification of species. Immediately after collection, the animals were transported to the laboratory of the Marine Biology Center of the University of Saõ Paulo (CEBIMar-USP) where they were maintained in plastic trays (50 cm length, 30 cm width, 20 cm height) with aerated seawater until examination. Each individual specimen was kept in a small perforated plastic flask (5.0 cm length, 3.2 cm diameter) to prevent possible aggressive interactions. Identification of the specimens was based on Holthuis (1955), Chace (1972), Williams (1984), and Christoffersen (1979, 1982, 1998). Determination of sex was based on the presence (males) or the absence (females) of the appendix masculina on the inner margin of the endopod of the second pair of pleopods. The carapace length (CL, from rostrum tip to

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MOSSOLIN ET AL.: POPULATION STRUCTURE OF ALPHEUS ARMILLATUS

Fig. 1. Location of study sites in the Saõ Sebastiaõ Channel.

the posterior dorsal margin) of each animal was measured with the aid of a digital caliper to the nearest 0.01 mm. Occurrence of ovigerous females was recorded, and eggs of each female were classified according to the embryonic development stage as: early (no evidence of compound eye development; yolk occupying 75-100% of egg volume), intermediate eyes developing as small, elongated, pigmented regions, yolk (occupying 5075% of egg volume), and late (with well-developed compound eyes; yolk occupying 25–50% of egg volume). After all measurements and observations were complete, animals were returned alive to their original environment, except for approximately 30 specimens from each study site that were randomly selected during the study period and deposited in the Museum of Zoology of the University of Saõ Paulo (MZUSP) under the registration numbers MZUSP 13719 (SF sample) and MZUSP 13720 (EA sample). Due to the low number of animals collected monthly at EA, analyses of temporal structure, growth, recruitment, and longevity were conducted on the dataset from the SF samples only. Because an initial data examination revealed occurrence of multiple cohorts, the following procedure was adopted to obtain the most objective definition of cohorts possible: a) Monthly CL data were distributed in 0.50 mm interval classes, which provided the clearest temporal sequence of CL class distributions. b) To emphasize frequency peaks that might correspond to cohorts, CL class distributions restructured by moving average (Bray and Pauly, 1986) were generated by the Elefan I routine of the FISAT II computer program (version 1.0.0, Gayanillo et al., 2002). c) Peak sequences that presented clear temporal progression along the CL classes were identified as cohorts. Only peaks corresponding to classes composed of two or more individuals (checked on the original distributions) and sequences of peak progression that could be followed for at least five months were considered in this step. Growth description was based on frequency distribution of CL classes and was conducted separately for males and females, according to the Von Bertalanffy equation:

Fig. 2. Temporal variation of temperature and salinity at Saõ Francisco ´ gua Beach (B) during the study period. Beach (A) and Engenho d’A

Lt ¼ L‘ ½1 ekðtt0 Þ

reproductive cycle. From this initial reference, relative ages in months were attributed to the frequency along the temporal sequence. The final adjustment of the Von Bertalanffy growth curve was performed on the CL (frequency peak) vs. time plot with the aid of the CurveExpert program (version 1.38, Hyams, 2001). Because of the occurrence of multiple cohorts in the present dataset, this procedure was preferred to that performed by the Elefan I routine because it considers only the cohorts data rather than any available frequency peak (as does Elefan I) for the curve adjustment. Longevity of each sex was estimated based on the largest CL class with frequency nearest to 99% from the overall distributions (13.0 mm for males and 14.0 mm for females).The other cohorts identified in step ‘‘c’’ were not included in the growth curve adjustment because they represented only segments of the temporal size progression and their inclusion in the analysis tended to cause under- or overestimation of the curve parameters. These cohorts were, however, essential in the recruitment cycle analysis in association with the reproductive cycle. All statistical analyses were based on procedures described by Zar (1996). Nonparametric procedures were adopted whenever the premises of the parametric tests were not fulfilled.

where Lt is the CL at time t, L‘ the asymptotic growth, K the growth constant, and t0 is the time at which Lt ¼ 0. Since t0 was not available, the iterative parameter search method available in the Elefan I routine was employed to perform a preliminary growth curve adjustment on the cohort that presented the longest sequence of frequency peak progression, and that was bred during the study period. This procedure aimed to estimate the approximated breeding time of this cohort by the projection of the obtained curve on the time scale. The adequacy of this estimation was checked with information on the

Environmental Conditions The study sites presented very similar conditions of surface water temperature conditions (Fig. 2) with values ranging from 208C (July 2000 and October 2001) to 308C (February

RESULTS

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Fig. 3. Overall carapace length (CL) frequency distribution of males (A) and females (B) of Alpheus armillatus from Saõ Francisco Beach.

Fig. 4. Overall carapace length (CL) frequency distribution of males (A) ´ gua Beach. and females (B) of Alpheus armillatus from Engenho d’A

2001) at SF (mean 6 s.d. ¼ 24.6 6 3.08C) and from 198C (August 2000) to 308C (January and April 2001) at EA (24.7 6 3.28C). While the temporal variation was clearly seasonal, temperature decreased more abruptly and tended to attain lower values in 2000 than in the following year. Conversely, the colder period was longer in 2001 than in 2000. Salinity also showed similar patterns at the two sites (Fig. 2), ranging from 31 ppt (December 2000 and January 2002) to 36 ppt (July 2000) at SF (33.5 6 1.3 ppt) and from 30 ppt (October 2000) to 36 ppt (March 2001) at EA (33.3 6 1.5 ppt). Although no significant negative correlation was verified with temperature (Spearman rs, P . 0.05), lower values tended to occur in the warmer months in which rainfalls are also more frequent in the region.

Overall Size Structure Overall frequency distributions of CL of males and females at SF and EA are presented in Figs. 3 and 4, respectively. The CL of males ranged from 4.8 mm to 13.7 mm (mean 6 s.d. ¼ 10.0 6 1.8 mm) at SF (Fig. 3A) and from 4.9 mm to 13.1 mm (10.3 6 1.5 mm) at EA (Fig. 4A). In females, CL ranged from 4.2 mm to 14.2 mm (10.3 6 2.1 mm) at SF (Fig. 3B) and 6.2 mm to 13.2 mm (10.7 6 1.5 mm) at EA (Fig. 4B). In both study sites, the size difference between sexes was significant (Mann Whitney U ¼ 136146; P ¼ 0.0005 for SF and U ¼ 8933.5; P ¼ 0.008 for EA). Conversely, sizes of each sex did not differ significantly between sites (U ¼ 36698; P ¼ 0.17 for males and U ¼ 38965; P ¼ 0.12 for females). Proportions of specimens in CL classes were also independent of the sites (contingency v2 ¼ 14.268; P ¼ 0.71143 for males and v2 ¼ 26.663; P ¼ 0.14503 for females).

Sex Ratio A total of 1113 shrimps were collected at SF, of which 547 were males and 566 were females. The same sampling effort yielded 145 males and 150 females at EA. The resulting sex ratio did not depart significantly from 1:1 in either sample (Yates corrected goodness-of-fit v2 ¼ 0.291; 0.50 , P , 0.75 for the SF sample and v2 ¼ 0.054; 0.75 , P , 0.90 for the EA sample).

Larval Release Periodicity Ovigerous females occurred throughout the year at both sites (Fig. 5). At SF their proportions ranged from approximately 80% to 100% during the whole study period except in May 2000 (61.1%) (Fig. 5A). A very similar temporal trend of high percentage of ovigerous females was

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2000-January 2001, June–July, 2001). However, the September–October 2001 hatching event observed at SF had no correspondent at EA.

Fig. 5. Monthly percentage of ovigerous females in the Alpheus armillatus samples from Saõ Francisco Beach (A) and from Engenho ´ gua Beach (B). Proportions of eggs in embryonic development stages I d’A (early stage), II (intermediate stage), and III (late stage) are distinguished. Labels represent the total number of ovigerous females in each month.

observed each month at EA, despite the small sample size in October 2000 and even the observed absence of females in samples from March and July 2000 (Fig. 5B). Because of the high percentage of ovigerous females found throughout the study period, hatching events were assessed by tracing variations of proportion of the eggs in each developmental stage, particularly the early and late stages, which were variable along the year. Six periods in which hatchings possibly predominated (April–May 2000, July–August 2000, December 2000-January 2001, June– July 2001, September–October 2001, and February 2002) were identified at SF during the whole study period (Fig. 5A). Correlation analyses (Pearson r) between the percentages of each egg stage and each of the environmental variables yielded a significant result (r ¼ 0.418; P ¼ 0.0423) in the test involving proportion of late eggs and water temperature only. Although this result should be interpreted with caution because it is marginally significant, it indicates that hatching was more intense in warmer months. Although the low number of animals collected prevented a detailed analysis of the hatching cycle at EA, the temporal variation of the proportion of late eggs in the November 2000-July 2001 period was very similar to that observed at SF, suggesting corresponding hatching events (December

Temporal Size Structure and Growth The temporal sequences of frequency distributions in CL classes of males and females from SF are presented in Fig. 6. Classes assigned as peaks are highlighted in the histograms. Four male cohorts could be followed: M1, from July (peak at 11.5 mm CL class) to November 2000 (12.5 mm), M2, from October 2000 (10.0 mm) to March 2001 (12.0 mm), M3, from October 2000 (7.0 mm) to July 2001 (12.5 mm), and M4 from August 2001 (9.0 mm) to January 2002 (11.5 mm). Three cohorts were identified for females: F1, from May (10.5 mm) to December 2000 (13.5 mm), F2, from October 2000 (10.5 mm) to March 2001 (12.0 mm), and F3, from December 2000 (9.5 mm) to August 2001 (13.5 mm). Although no clear peak progression could be associated with them, recruitment events were also verified in March and August 2001, and in February 2002. Growth analyses were conducted on cohorts M3 and F3. Preliminarily adjusted growth curves (also represented in Fig. 6) indicated that both cohorts were originated from the same reproductive event. The former cohort was four months old when first identified (October 2000), while the latter was six months old (December 2000). The adjusted curves (Fig. 7) are described by the equations Lt ¼ 13.90(1 e2.28t) and Lt ¼ 15.34(1 e1.89t) for males and females, respectively. The growth pattern of both sexes were similar, with males tending to grow more rapidly (higher K) and to attain smaller sizes (lower L‘) than females (Fig. 7). Approximate breeding times of the male and female cohorts originated during the study period (M2 to M4, F2 and F3) were estimated in accordance to the respective growth model and are presented in Table 1. For all cohorts except M2, the breeding time fell in a month previous to one of the hatching periods described in the previous section. The breeding time of cohort M2 (April 2000) coincided to the hatching period of April–May 2000. The estimated longevity of males and females was 1.20 years (14.4 months) and 1.29 years (15.5 months), respectively. Animals with larger CL’s comprised very low proportions of the specimens and were concentrated in cohorts recruited prior to the study period (Fig. 6). DISCUSSION A sex ratio that does not depart significantly from 1:1 has been verified in other snapping shrimp species such as Alpheus dentipes (see Fernańdes-Munõz and Garcia-Raso, 1987), Betaeus emarginatus (H. Milne Edwards, 1837) (see Lardies et al., 1998), and A. angulatus McClure, 1995 (see Mathews, 2002). This has been attributed to the formation of male and female pairs that commonly occur in alpheid species (Young, 1986; Erdman and Blake, 1987; FernańdezMunõz and Garcia-Raso, 1987; Werding, 1990; Lardies et al., 1998; Mathews, 2002). During the fieldwork conducted in present study, pairs of A. armillatus were commonly observed after rocks were removed from the substrate. The same behavior was also observed in a population of A. armillatus in Cuba (Martinez-Iglesias et al., 1996–1997).

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Fig. 6. Temporal sequence of frequency distributions in CL classes of males and females of Alpheus armillatus from Saõ Francisco Beach. Labels to the right of each histogram represent the number of data in the sample. Dark bars are peaks obtained form the restructured frequency distribution. Thin lines were used to illustrate temporal peak progression of male and female cohorts (M1 to M4 and F1 to F3, respectively). Thick lines represent the preliminary growth curves fit on cohorts M3 and F3 for estimation of the approximate breeding time of the cohorts.

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Table 1. Approximated hatching times of male (M2 to M4) and female (F2 and F3) cohorts of Alpheus armillatus from Saõ Francisco Beach estimated by the respective growth curve equations. Males

Cohort

Month of detection

CL (mm)

Females Estimated breeding time

Cohort

Month of detection

CL (mm)

Estimated breeding time

M2 October/00 10.0 April/00 F2 October/00 10.5 March/00 M3 October/00 7.0 June/00 F3 December/00 9.5 June/00 M4 August/01 9.0 February/01

Fig. 7. Growth curves of males and females of Alpheus armillatus from Saõ Francisco Beach. Data from cohorts M3 and F3 with ages attributed according to the preliminarily adjusted curves (see Fig. 6).

The nearly 1:1 sex ratio and the overall size class distributions indicate that pairs are formed by individuals of similar size with females slightly larger than males. This condition was in fact observed during sampling and has also been verified in populations of A. schmitti Chace, 1972 (see Werding, 1990), and of A. angulatus (see Mathews, 2002). Occurrence of pairs in which the female is markedly larger than the male has been reported for A. heterochaelis and A. normanni Kingsley, 1878 (see Nolan and Salmon, 1970). While ovigerous females occurred in high proportions throughout the year, A. armillatus presented three main larval release periods in a year at SF and possibly at EA as well. This was possibly related to higher temperatures that would favor development and growth of larvae (Sastry, 1983). At SF the identified cohorts were associated with three such periods (M2 and F2 associated with April–May 2000, M3 and F3 with July–August 2000, and M4 with March 2001). The location of the breeding time before the corresponding hatching period is in accordance to the growth model, because these points represent the origin of the curves where Lt ¼ 0. The coincident breeding time and larval release period in cohort M2 suggest a slight overestimation of growth parameters for this cohort. Continuous reproduction and multiple annual recruitments were also verified in A. normanni in seagrass meadows of Puerto Rico (Bauer, 1989). In other studies of recruitment in snapping shrimp populations, it has been shown that the pattern can be markedly seasonal (in Synalpheus fritzmuelleri and S. apioceros; Felder, 1982) or continuous, with higher intensity in the warmest months of the year (in S. longicarpus, S. brooksi, and S. pectiniger; Erdman and Blake, 1987). The recruitment pattern of the A. armillatus population from the Saõ Sebastiaõ channel is more similar to the latter three species, although no clear difference in intensity was observed between warm and cold seasons. According to the growth curves obtained, the smallest A. armillatus sampled were two to three months old. The occurrence of individuals smaller than those (see Materials

and Methods) indicates that settlement occurred earlier than that. Duration of larval development time in snapping shrimp has been estimated to be two to three weeks in A. armillatus, A. normanni, and Synalpheus hemphilli Coutie`re, 1909 (see Knowlton, 1973), 14 to 25 days in A. ruber, and 32 days in A. macrocheles (see Lebour, 1932). Fernańdez-Munõz and Garcia-Raso (1987) verified that postlarvae of A. dentipes settled in the substrate (the calcareous algae Mesophyllum lichenoides (Ellis) Lemoine 1928) after a 2–3 month period of larval development. The 14–15 month lifespan estimated for A. armillatus in the present study is similar to that of A. dentipes (see Fernańdez-Munõz and Garcia-Raso, 1987), the only other Alpheus species for which information of this sort exists. The small number of individuals larger than the estimated maximum size (13.0 mm for males and 14.0 mm for females) that were occasionally sampled represent animals that lived longer than the majority, performed an extra molt or presented a larger size increment in the previous molt.

ACKNOWLEDGEMENTS The authors express their sincere gratitude to FAPESP (Fundaçaõ de Amparo a` Pesquisa do Estado de Saõ Paulo) for providing a scholarship grant (99/10283-0) to one of us (ECM), to CEBIMar-USP, for providing all logistical assistance and laboratory facilities in Saõ Sebastiaõ, and to the Comissaõ de Po´s-graduaçaõ, area Zoology, of the Instituto de BiocieˆnciasUSP for their kind assistance in providing laboratory equipment and materials. Finally, we are also deeply grateful to all personnel and friends at the Departamento de Zoologia and Departamento de Ecologia of the Instituto de Biocieˆncias-USP. The text also benefited from comments and suggestions of the two anonymous referees of the Journal of Crustacean Biology.

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