Introduction
Family Alpheidae Rafinesque, 1815 is one of the richest taxonomic groups among caridean shrimp accounting for more than 700 species, which are distributed in approximately 50 genera and exhibit high morphological diversity (Bauer, Reference Bauer2023); these species also stand out for their geographic and ecological distribution, worldwide (Anker et al., Reference Anker, Ahyong, Noël and Palmer2006; Anker, Reference Anker2020, Reference Anker2022; Chow et al., Reference Chow, De Grave, Anker, Poon, Ma, Chu, Chan and Tsang2021). Alpheus Fabricius, 1978 and Synalpheus Spence Bate, 1888 are the most species-rich genera based on specific morphological and behavioral features (Bauer, Reference Bauer2023).
The most distinctive morphological feature in both Alpheus and Synalpheus is heterochely in the first pair of chelipeds: one cheliped is modified into an enlarged ‘snapping claw’ where as the other one has the typical morphology of a cutting or gripping appendage (Bauer, Reference Bauer2023). The typical snapping claw movement turned into one of the most representative sounds of biological noises in shallow marine waters. The snapping-claw mechanics is explained by a remarkably fast movement of the dactylus, which introduces a plunger structure into the propodus'cavity (Versluis et al., Reference Versluis, Schmitz, Heydt and Lohse2000; Patek and Longo, Reference Patek and Longo2018). This interaction produces a straightforward water jet stream that produces the characteristic ‘pistol’ sound which, in its turn, remains one of the popular names attributed to these species (Au and Banks, Reference Au and Banks1998; Schmitz, Reference Schmitz and Wiese2001; Kim et al., Reference Kim, Hahn, Choi and Kim2010).
Studies in the literature address the use of the ‘pistol’ or ‘snapping’ strategy, for different purposes, by the investigated species throughout their life (Knowlton and Moulton, Reference Knowlton and Moulton1963; Knowlton and Keller, Reference Knowlton and Keller1982; Hughes, Reference Hughes1996; Lee et al., Reference Lee, Choi, Shin and Song2021). However, it is mostly defined as signals emitted in conspecific communication and interspecific interactions, such as in agonistic behaviours, since they can stun their pray with the snapping sound, and many of them behave aggressively in the process to protect their cryptic crevices (Bohnenstiehl et al., Reference Bohnenstiehl, Lillis and Eggleston2016).
In members of the genus Synalpheus the snapping behaviour gains a unique significance because some species exhibit eusocial colony organization within sponges (Duffy et al., Reference Duffy, Morrison and Ríos2000). Communication and colony defence are significant examples of snapping behaviour in these populations (Duffy et al., Reference Duffy, Morrison and Macdonald2002). Synalpheus can be divided into two informal groups, namely: gambarelloides (mandatory symbionts of sponges) and non-gambarelloides (free-living or facultative symbionts found in biogenic substrates, without eusocial condition, as the S. fritzmuelleri) (Ríos and Duffy, Reference Ríos and Duffy2007; Anker and De Grave, Reference Anker and De Grave2008). All records available in the literature about cheliped morphology and Synalpheus snapping behaviour are associated with specimens belonging to the eusocial gambarelloides group (Duffy, Reference Duffy1996; Duffy et al., Reference Duffy, Morrison and Macdonald2002; Tóth and Duffy, Reference Tóth and Duffy2008).
Heterochely variation in eusocial populations of Synalpheus species has been described in the literature (Duffy and Macdonald, Reference Duffy and Macdonald1999). This variation is mainly observed in the colony's reproductive ‘queens’, who spend more energy in reproductive activities and often present both minor chelipeds, whereas the colony's ‘helper’ shrimps present the major snapping cheliped developed for both host and colony defense purposes (Chace, Reference Chace1972; Duffy and Macdonald, Reference Duffy and Macdonald1999). On the other hand, according to studies available in the literature, lack of heterochely in non-eusocial species appears to be quite rare (Pearse and Govind, Reference Pearse and Govind1987; Anker et al., Reference Anker, Ahyong, Noël and Palmer2006).
There are, at least, three studies about specimens with two major chelipeds available in the literature, mainly in Alpheus species (Darby, Reference Darby1939; McClure, Reference McClure1996; Soledade et al., Reference Soledade, Oliveira and Almeida2017). Moreover, interpretations about the mechanism inducing symmetry in natural conditions remain poorly explored. With respect to Synalpheus, there is only a brief description of one misidentified specimen available in the literature, and it does not provide any discussion about it (Hickman and Zimmerman, Reference Hickman and Zimmerman2000).
The Synalpheus fritzmuelleri Coutière, 1909 is one of the most abundant non-gambarelloides species belonging to genus Synalpheus and it is widely distributed in the Atlantic Ocean (Anker et al., Reference Anker, Tavares and Mendonça2016). It is often found in Brazilian waters and in association with several invertebrates, such as sponges and corals, besides found free-living in consolidated substrates (Almeida et al., Reference Almeida, Terossi, Buranelli, Castilho, Costa, Zara and Mantelatto2018). Despite its ubiquitous nature, little is explored about this species' biology and behaviour, although it is often found as ‘pair-bond’ in different types of living or non-living substrates (Almeida et al., Reference Almeida, Santos, Soledade, Santos and Pérez2015).
The aims of the present study were to register – for the first time – a S. fritzmuelleri specimen presenting symmetric major chelipeds, as well as to address the consequences of this abnormality for the investigated species' natural life and behavior.
Materials and methods
Sampling procedures were conducted between October 2022 and May 2023, at Cais do Porto [docks] region, Itaguá Bay, Ubatuba City, São Paulo State, Brazil (23°27′05″ S; 45°02′48″ W).
Specimens were sampled in symbiosis with bryozoan biogenic substrate Schizoporella sp., which adhered to the pilings of the docks, at maximum depth of 4 m. All sampling procedures were performed through free-diving activities always carried out at day time.
Bryozoan fragments were carefully sampled with the aid of a small diving knife and stored in plastic bags. All biogenic substrates were carefully examined to investigate the incidence of caridean shrimp within their pores. All symbiotic species were identified in a laboratory environment; S. fritzmuelleri specimens were isolated, photographed, and measured to enable morphological comparisons between those presenting normal features and the ones carrying abnormalities.
The following measurements were taken from all specimens in good condition (with all chelipeds intact): Carapace Length (CL); Major Cheliped Length (MaCL), Major Cheliped Width (MaCW); Minor Cheliped Length (MiCL); and Minor Cheliped Width (MiCW).
All measurements were taken with a stereomicroscope (Zeiss Stemi SV6, fitted with Zeiss Stemi 2000-C image capture system) equipped with a camera and with AxioVisio software (version 4.8). Pictures of both major structures and body plan were taken using a stand and semiprofessional Nikon Coolpix P100 camera at 26x optical zoom.
The abnormal specimen was deposited in the Crustacean Collection of the Biology Department (CCDB) of FFCLRP, University of São Paulo, Ribeirão Preto City, Brazil (CCDB/FFCLRP/USP – Authorization n. 071/2012/SECEX/CGEN): CCDB 7556.
Results
In total, 34 caridean shrimps were recorded in association with the biogenic substrate; 20 of them belonged to species S. fritzmuelleri. Thirteen specimens of the target species presented both chelipeds intact for measurement purposes, whereas one presented symmetry of the major claw.
Regular specimens ranged from 1.30 to 6.02 mm CL, whereas major cheliped size ranged from 2.65 to 8.87 mm, in length, and from 0.98 to 4 mm, in width. Minor cheliped ranged from 1.06 to 3.42 mm, in length, and from 0.38 to 1.14 mm, in width (mean values are described in Table 1). Anomalous species' major cheliped was 4.18 mm long and 1.71 mm wide, whereas their minor cheliped was 3.39 mm long and 1.28 mm wide.
Table 1. Morphological approaches by specimens of Synalpheus firtzmuelleri Coutière, 1909 associated with bryozoarian substrates at Ubatuba Bay, SP, Brazil
MaCL, major cheliped length; MaCW, major cheliped width; MiCL, minor cheliped length; MiCW, minor cheliped width.
Regular conditions indicate specimens with heterochely and abnormality condition indicates the specimen with symmetric chelipeds.
All measures are indicated in millimetres (mm).
All morphological features observed for the investigated specimen were classified as normal for regular Synalpheus individuals, except for lack of heterochely. Details about the investigated species' overall morphology, and comparison between regular and symmetric S. frizmuelleri morphology are shown in Figure 1 (panoramic image) and Figure 2 (cheliped details).
Figure 1. Overall view of the entire body of Synalpheus fritzmuelleri Coutière, 1909 specimen with regular conditions and with symmetric chelipeds. (A) dorsal view of the specimen with abnormality in symmetric chelipeds; (B) dorsal view of the specimen with regular asymmetric chelipeds; The white arrow points to differences in minor asymmetric cheliped and anomalous structure (C) Lateral view of the specimen with symmetric chelipeds; (D) Ventral view of the specimen with symmetric chelipeds. Scale bar: 1 cm.
Figure 2. Image detail showing Synalpheus fritzmuelleri specimen, with emphasis on the symmetric cheliped. (A) lateral view; (B) dorsal view. Scale bar: 1 mm.
Discussion
The present study provides for the first time a record of an abnormality in the symmetry of both major chelipeds in S. fritzmuelleri. Abnormalities and uncommon structures' growth, mainly after ecdysis processes in crustaceans, are not rare. They have been reported in several groups, namely: extra claws, in crayfishes (Nakatani et al., Reference Nakatani, Okada and Yamaguchi1997); multiple morphological deformations, in Penaeoidea shrimps (Betancourt-Lozano et al., Reference Betancourt-Lozano, Baird, Sangha and González-Farias2006; Béguer et al., Reference Béguer, Pasquaud, Noël, Girardin and Boët2008), as well as growing deformation in the cheliped of some Brachyura crabs (Ramírez-Rodríguez and Félix-Pico, Reference Ramírez-Rodríguez and Félix-Pico2010). Most study results and reports available in the literature focused on isolated cases, like the one reported in the present study, according with, only one or just a small number of specimens in the investigated populations presented physical anomalies.
It is common to find situations requiring cheliped autotomy or amputation in snapping shrimps, either from in a fight or escape from predators. Whenever autotomy takes place in the major snapping claw, the pincer (or minor claw) undergoes significant transformation into a new major cheliped (Young et al., Reference Young, Pearse and Govind1994; Pereira et al., Reference Pereira, Tracey, Cooney, Korey and Hughes2014). The transformation of the minor cheliped into snapping claw happens exactly one moult cycle after the loss of the original appendix (Read and Govind, Reference Read and Govind1997). Studies available in the literature advocate that this process takes place because the minor cheliped is likely to be the suppressed major structure, and that when the major cheliped is missing, a specific gene is activated to turn the minor claw into a major claw (Stephens and Mellon, Reference Stephens and Mellon1979).
The two-major-chelipeds condition in specimens belonging to family Alpheidae is extremely rare, and this condition seems enables neutral or impossible the reversal control to an asymmetric morphology. Soledade et al. (Reference Soledade, Oliveira and Almeida2017) observed symmetry in Alpheus specimens and suggested at least three hypotheses capable of explaining the observation of this condition in the investigated animals: (1) symmetry was developed at the juvenile stage due to genetic inhibition of the mechanism accounting for developing asymmetric chelipeds; (2) symmetry was generated at the adult stage, after a single case of major cheliped autotomy and the minor cheliped's non-transformation into a snapping claw; and, finally, (3) after the adult specimen was autotomized and lost the major cheliped, it was sampled during the ‘asymmetry reversal process’, that is the process responsible to maintain the heterochely when some of the chelipeds are lost or are being formed.
Based on the CL size of the herein investigated S. fritzmuelleri specimen, one can say that it was likely a juvenile. Its major cheliped was also smaller than the mean size observed for other specimens in the same population, whereas the minor cheliped was considered bigger than that of other individuals due to symmetry, as shown in Figure 1. The first hypothesis suggested by Soledade et al. (Reference Soledade, Oliveira and Almeida2017) appears to be herein corroborated, since the symmetry observed for the investigated Synalpheus specimen can result from the genetic inhibition of snapping claws' development.
It is important registering cases like this, since they present a rare condition in Synalpheus species; moreover, discussions about these anomalies can drive evolutionary assessment to be conducted in the future.
Acknowledgements
We are grateful to all our laboratory colleagues and co-workers, for the help provided during sampling and analysis processes. We would also like to thank ‘Instituto Chico Mendes de Conservação da Biodiversidade’ (ICMBio) and ‘Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis’ (IBAMA), for allowing sample collection. The authors thanks the contributions made by the two reviewers that improved the quality and scientific contribution of this manuscript.
Authors' contributions
Isabela Ribeiro Rocha Moraes: Sampling, main text writing, bibliography observation, photograph taking and edition. Larissa Zacari: First abnormality observation, measurements, bibliography observation, formal manuscript revision. Rafael de Carvalho Santos: Main text revision, English grammar correction, bibliography observation. Gabriel Felipe Rodrigues: Sampling, main text revision, English grammar correction, bibliography observation. Antonio Leão Castilho: Samples' coordination, text writing, photograph taking and full text revision. He also secured the funding that made the current study possible.
Financial support
This project was funded by ‘Conselho Nacional de Desenvolvimento Científico e Tecnológico’ (CNPQ Grant PQ 311034/2018-7), ‘Coordenação de Aperfeiçoamento de Nível Superior – CAPES’, Brazil (CAPES PRINT 88881.310767/2018- 01, CAPES PROEX 23038.000802/2018-25).
Competing interest
None.
Ethical standards
Besides working with invertebrates, all ethical standards were applied, with licenses and procedures conducted in the best way possible for this work.
Data availability
The data that support the findings of this study are available from the corresponding author, IRRM, upon reasonable request. The abnormal specimen was deposited in the Crustacean Collection of the Biology Department (CCDB) of FFCLRP, University of São Paulo, available for consultation by number: CCDB 7556
