Biological and ecological notes about the snapping shrimp Alpheus formosus Gibbes, 1850 from two continental islands in São Paulo State - Brazil

Abstract

While previous studies on Alpheus formosus Gibbes, 1850 focused on taxonomic and phylogenetic issues, the present study provides information on the biology and ecology of this snapping shrimp, a representative coral reef species widely distributed in the Atlantic Ocean. We studied A. formosus between 2015 and 2016 on two islands in São Paulo state, Brazil: Laje de Santos and Vitoria Island. We analyzed 47 specimens from Laje de Santos and 44 from Vitoria Island. Individuals ranged in size from 2.0 mm to 13.99 mm CL. The mean number of embryos attached to the pleopods of females was 211.28 ± 312.8 in Laje de Santos and 125.2 ± 177.8 in Vitoria Island. This species should be included in monitoring programs of coral ecosystems they inhabit as A. formosus represents a key element in trophic dynamics of these ecosystems.

Keywords
Caridean shrimps; consolidated substrate; ecology; population structure; preserved areas

INTRODUCTION

The shrimps from the Family Alpheidae are morphologically and ecologically diverse (Bauer, 2004), and are widely distributed with more than 600 species described thus far (De Grave and Fransen, 2011). The genus Alpheus Fabricius, 1798 represents almost half of the species comprising the family (Kim and Abele, 1988; Bracken-Grissom and Felder, 2014; Anker et al., 2015). These shrimps are mostly found in tropical and subtropical marine ecosystems (Chace, 1988) inhabiting a wide variety of niches, from tidal pools in estuaries to deep-sea regions (Anker et al., 2006). Representatives of Alpheidae can also live in mutualistic or commensal associations with other decapods, fishes, sponges, and anemones (Boltaña and Thiel, 2001; Bauer, 2004; Anker et al., 2006).

Although Alpheus is the most representative genus of its family (Anker et al., 2006; De Grave and Fransen, 2011), studies about its population biology are scarce compared to knowledge about its taxonomy and diversity. This could be due to the presence of several species complexes (Mathews and Anker, 2009; Costa-Souza et al., 2018) and because these species are ecologically enigmatic (Felder, 1982), which according to Costa-Souza et al. (2018) makes monthly sampling difficult and contributes to the lack of knowledge about this group. Alpheus formosus Gibbes, 1850 can be found in most of the Western Atlantic: Bermuda, North Carolina, Florida, Gulf of Mexico, Bahamas, West Indies, Central America, Colombia, and Venezuela (Christoffersen, 1998; Cunha et al., 2015; Anker et al., 2016).

On the Brazilian coast, it is very common at Atol das Rocas, Fernando de Noronha and from Ceará to Santa Catarina (Christoffersen, 1998; Anker et al., 2008; 2016; Soledade and Almeida, 2013; Cunha et al., 2015). Although A. formosus is abundant on the Brazilian coast, there are few studies about its biological and ecological features. The present study aims to elaborate a brief description of some aspects of the biology and ecology of A. formosus from two conservation areas in São Paulo state: Laje de Santos and Vitoria Island.

MATERIAL AND METHODS

Sampling

The shrimps were collected quarterly between June 2015 and June 2016 in two different island regions: The Marine State Park of Laje de Santos (MSPLS) and Vitoria Island (Fig. 1). The specimens were sampled in both regions using a combination of techniques, i.e., employing active search by two divers equipped with SCUBA for 1 hour each per diving session, and using Artificial Substrates of Refuge (ASR). The ASR consists of a plastic net structure in a 25 ( 25 ( 25 cm (height x length x depth) cube shape filled with plastic tubes and small plastic nets as previously described by Alves et al. (2019) and da Silva et al. (2018). Five ASR were installed in both islands on a rocky surface and removed three months later.

Figure 1.
Location of the two continental islands, São Paulo State, Brazil, where the sampling was conducted for the present study (2015-2016).

The specimens collected were bagged individually in situ and frozen to preserve color and morphological integrity. Subsequently, they were transferred to the laboratory and identified according to specialized taxonomic keys (Anker et al., 2008; Soledade and Almeida, 2013).

Population Structure and Reproduction

The carapace length (CL) of shrimps was measured under an imaging system of the stereoscopic microscope (Zeiss STEMI V6) from the orbital hood to the posterior margin of the carapace, and individuals were grouped in 2 mm size-class intervals to evaluate and visualize the population structure. The animals were sexed according to the presence (males) or absence (females) of the appendix masculina on the endopodite of the second pair of pleopods, and also gonopore positions (Bauer, 2004). The reproductive season was assessed by observing the presence of ovigerous females (females with eggs/embryos adhered to their pleopods) during the sampling period. For further comparisons, the seasons were classified as winter (June), spring (September), summer (January) and autumn (March) according to Sant’Anna Neto (2005). A chi-square test was performed to evaluate the differences in the distribution of the demographic groups (males, non-ovigerous females, and ovigerous females) between the seasons on both islands.

In order to evaluate the number of embryos attached to the female pleopods, only females with non-damaged embryos were selected, and embryos were counted with a manual counter. Embryos were categorized into two embryonic developmental stages: Stage I, with no eyes formed, and Stage II, with evident eyes formed (see Corey and Reid, 1991). Considering the low number of females carrying embryos in Stage I and II, we provide the mean embryo number of A. formosus ovigerous females, and no statistical analyses were performed to compare mean values between stages.

RESULTS

We collected 47 specimens in Laje de Santos and 44 in Vitoria Island. All specimens identified in the present study presented a variable “dark brown-red background”, sometimes with a more yellowish tone; the distinctive dorsal white longitudinal band, however, was a consistent characteristic that did not vary among specimens from both islands (Fig. 2).

Figure 2.
Alpheus formosus: color pattern from individuals collected at Laje de Santos and Vitoria Island, São Paulo State, Brazil (2015-2016). (A) Lateral view; (B) dorsal view.

At Laje de Santos (Fig. 3), shrimp abundance peaked in spring with total of 23 individuals: males were predominant with 13 specimens sampled; non-ovigerous females were abundant in summer and absent in autumn; ovigerous females were absent in the summer and highest abundance was observed in spring. The Chi Square test showed the following abundance differences: Summer non-ovigerous Females ( Ovigerous Females (p=0.0015), and Summer Ovigerous Females ( Males (p=0.014).

Figure 3.
Abundance of Alpheus formosus individuals during all seasons (2015-2016) collected at Laje de Santos, São Paulo State, Brazil.

On Vitoria Island (Fig. 4), the snapping shrimps were more abundant during spring and autumn. Males were found during all sampling periods, and were most abundant in autumn. Non-ovigerous females were most abundant in spring with nine specimens and were absent in summer and winter. Ovigerous females were most present in winter and autumn with three specimens sampled in each season, and absent in the summer. The results of the Chi Square test revealed differences in abundance in spring for Non-ovigerous Females ( Ovigerous Females (p=0.011).

Figure 4.
Abundance of Alpheus formosus individuals during all seasons (2015-2016) collected at Vitoria Island, São Paulo State, Brazil.

In Laje de Santos, specimens ranged in size classes from 2 mm CL to 13.99 mm CL, with the 4.0-5.99 mm CL size class predominating. Non-ovigerous females were mainly found in the size classes of 4.0-5.99 mm CL and 6.0-7.99 mm CL, males in the size class 4.0-5.99 mm CL, and ovigerous females in 6.0-7.99 mm CL and 8.0-9.99 mm CL (Fig. 5). In Vitoria Island, common size classes ranged from 2 mm CL to 11.99 mm CL, and the 4.0-5.99 mm CL size class contained most of the analyzed individuals, including males and non-ovigerous females. Most ovigerous females were present in the size class 10.0-11.99 mm CL (Fig. 6).

Figure 5.
Size-class distribution of Alpheus formosus collected at Laje de Santos, São Paulo State, Brazil.

Figure 6.
Size-class distribution of Alpheus formosus individuals collected at Vitoria Island, São Paulo State, Brazil.

Ovigerous females from Laje de Santos (N = 7) ranged in size from 5.98 mm to 12.22 mm CL; four individuals carried embryos in Stage I, the other three females had Stage II-embryos attached. The number of embryos ranged from six (final stage) to 847 (initial stage); mean embryo number for Laje de Santos was 211.2 ± 312.8. In Vitoria Island, seven ovigerous females were collected, but we counted the embryos of only four of them due to the degradation of embryos in the other three specimens. Female sizes ranged between 6.06 mm to 11.51 mm CL with all embryos in Stage II; embryo number ranged from 2 to 383 (mean 125.2 ± 177.8).

DISCUSSION

The color pattern of the snapping-shrimp A. formosus resembles the other conspecific shrimp: Alpheus panamensis Kingsley, 1878 (previously considered junior synonym of A. formosus). The color of A. formosus is very particular with a characteristic “dark brown-red” background, a broad yellow band running mediodorsally from the tip of the rostrum to the telson, a narrow and irregular white longitudinal band on each side of the abdomen, and bluish to purplish walking legs (Anker et al., 2008). Even though the specimens sampled in this study showed variations in their dark brown-red background color patterns, the other characteristics described above were similar.

Among the caridean shrimps, A. formosus is one of the most common snapping shrimps in American tropical waters (Kim and Abele, 1988). In Laje de Santos and Vitoria Island, our results suggest well-established populations because all demographic groups were sampled across the seasons with an abundance peak in the spring, despite the low number of specimens. On the southeastern Brazilian coast, abundance peaks of decapods (Negreiros-Fransozo and Fransozo, 1992; Lima et al., 2014; da Silva et al., 2018) are associated with the warmer seasons (spring and summer) characterized by nutrient-rich water masses and high primary production (Schettini et al., 1998; Sant’Anna Neto, 2005). These favorable environmental conditions may explain the elevated number of A. formosus, especially during spring (Figs. 3, 4).

Ovigerous females of almost all size classes were found in both localities, presenting larger sizes than males and non-ovigerous females. This pattern of larger ovigerous female is expected since embryos adhere to the pleopods in a lateral cavity formed between the first and third pleura, which enlarge as the female grows. Therefore, larger females would have more space to carry embryos, and consequently, higher fecundity rates (Corey and Reid, 1991; Clarke, 1993; Bauer, 2004).

In both sampling locations, ovigerous females were mostly found from the 6 mm CL onwards, which agrees with the pattern found for many alpheid shrimps especially with other conspecific Alpheus spp. (Corey and Reid, 1991; Pavanelli et al., 2008; 2010; Harikrishnan et al., 2010; Costa-Souza et al., 2014; Pescinelli et al., 2016).

The mean number of embryos attached to pleopods of A. formosus is relatively low when compared to similar-sized congeners. The maximum number of embryos attached to pleopods of A. formosus observed is close to those of species with more than 11 mm CL (Bauer, 1991; Corey and Reid, 1991; Pavanelli et al., 2008; 2010; Harikrishnan et al., 2010; Costa-Souza et al., 2014; Pescinelli et al., 2017). Such inter- and intraspecific variation is related to genetic and environmental (temperature, salinity, photoperiod) factors (Sastry, 1983).

Being a common species in coral reefs and rocky bottoms, A. formosus is a key element in trophic dynamics of these ecosystems (Chace, 1972; Wenner and Boesch, 1979; Anker et al., 2008). Therefore, knowledge about its ecology is important to understand the trophic interactions in these valuable ecosystems. A monitoring program of this species and the ecosystem should be implemented to properly assess local conditions, which may help to develop adequate management tools for conservation purposes.

ACKNOWLEDGEMENTS

The authors would like to thank the funding provided by FAPESP Process 2015/01959-5 to conduct this work. Additionally, this study was partially financed by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brazil (CAPES; financial code CAPES/CIMAR II 23038.004310/2014-85, 0687/2018 PROEX 23038.000802/2018-25 and CAPES PRINT 88881.310767/2018-01). We also thank all members of NEBECC and LABCAM who participated during the sampling periods and helped to finish this paper.

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Publication Dates

• Publication in this collection
  05 Aug 2020
• Date of issue
  2020

History

• Received
  16 Jan 2020
• Accepted
  15 May 2020