Introduction
Members of the infraorder Axiidea represent a significant component of the macroinfauna in sandy intertidal and subtidal environments, exhibiting a cosmopolitan distribution. Over recent decades, taxonomic revisions of burrowing decapods have been driven by molecular genetic investigations, as well as studies exploring their morphological nuances, physiology, behaviour, reproductive biology, and population dynamics (Kornienko, Reference Kornienko2013). Despite these advancements, identifying and documenting species distributions remain crucial for elucidating biogeographical patterns and ecological dynamics.
Audacallichirus mirim (Rodrigues, 1971) was first described by Sérgio de Almeida Rodrigues as Callianassa (Callichirus) mirim. During the 1990s, it was reclassified as Sergio mirim (Pezzuto, Reference Pezzuto1998), and its current scientific nomenclature, Audacallichirus mirim, is now widely accepted (Hernáez et al., Reference Hernáez, Pinheiro, Almeida Alves-Junior and Santana2022b). Audacallichirus mirim belongs to the group commonly known as ‘burrowing shrimps’ which inhabit soft sediments mainly in intertidal and subtidal regions, although some species extend to deeper habitats (Kensley, Reference Kensley1996; Felder and Kensley, Reference Felder and Kensley2004; Dworschak et al., Reference Dworschak, Felder, Tudge, Thiel and Watling2012). These ghost shrimps are notable for constructing burrows that vary in shape and depth (Griffis and Suchanek, Reference Griffis and Suchanek1991; Pereyra and Carvalho, Reference Pereyra and Carvalho2020) and for their significant influence on community structure (Pillay, Reference Pillay2019). Their burrowing activities, involving the removal of water and sediment, contribute to bioturbation, thereby enhancing the suspension of organic matter and pollutants, nitrogen fixation, and food availability across trophic levels (Ziebis et al., Reference Ziebis, Forster, Huettel and Jorgensen1996; Bertics et al., Reference Bertics, Sohm, Treude, Chow, Capone, Fuhrman and Ziebis2010).
The ghost shrimp A. mirim has previously been recorded along the Brazilian coast, from Bahia to Rio Grande do Sul, by Hernáez et al. (Reference Hernáez, Pinheiro, Almeida Alves-Junior and Santana2022b). However, these authors did not record this species in certain mesoregions of southeastern Brazil. This study marks the first report of the species in southern Espírito Santo and northern Rio de Janeiro.
Materials and methods
The fieldwork was conducted in March 2023. Initially, the focus of the study was to investigate the populations of Callichirus corruptus (Hernáez et al., Reference Hernáez, Miranda, Rio and Pinheiro2020a) along the southeastern coast of Brazil. During our campaigns, we captured two male specimens of Audacallichirus mirim at two different beaches: Piúma Beach, located in Piúma municipality in the southern Espírito Santo state (20°50′42.11″S and 40°44′16.04″W) and Guaxindiba Beach, located in São Francisco do Itabapoana municipality in the northern Rio de Janeiro state (21°28′42.41″S and 41°3′24.57″W). This marks the first record of the species in both the regions (Figure 1).
Figure 1. Audacallichirus mirim collection area in southern Espírito Santo (Piúma Beach (A)) and northern Rio de Janeiro states (Guaxindiba Beach (B)).
At each locality, burrowing shrimp specimens were collected from their burrows using a steel suction pump (diameter = 80 mm, length = 100 cm) within the intertidal zone (depth ~80 cm). The pump was applied up to five times in each burrow for extraction. After collection, each specimen was carefully rinsed with seawater, placed in a plastic bag, preserved in ice, and subsequently examined. Abiotic conditions were measured at both the surface water and within the galleries, including temperature, pH, conductivity, salinity, and dissolved oxygen using a multiparameter probe (U-50 series, Horiba, Japan).
In a laboratory, each specimen was identified, and its sex was determined based on the morphology of the first pair of pleopods. In cases where this criterion failed to allow definitive sex determination, the location of gonopores and life stage (adult or juvenile) was revisited (Hernáez, Reference Hernáez, Türkoğlu, Önal and Ismen2018). Systematic identification was based on studies of Poore et al. (Reference Poore, Dworschak, Robles, Mantelatto and Felder2019) and Hernáez et al. (Reference Hernáez, Pinheiro, Almeida Alves-Junior and Santana2022b), supplemented by taxonomic classification resources available at https://www.marinespecies.org/index.php. The biometric measurements recorded for each specimen included total length (mm), cephalothorax length (mm), left cheliped length (mm), left cheliped width (mm), right cheliped length (mm), right cheliped width (mm), and total weight (g).
Sediments of each sandy beach were collected using a shovel, stored in plastic bags and transported to the laboratory. Aliquots of each sample (<2.0 mm) was dried in an oven at 60°C and then separated for granulometric measurements without removing carbonates and organic matter. This determination was performed using a Shimadzu Series SALD-3101 laser diffraction particle size analyzer. The diameter of grain size (mm) was classified according to the scale of the Massachusetts Institute of Technology (Wentworth, Reference Wentworth1922): very coarse sand (2 to 1 mm); coarse sand (1 to 0.5 mm); medium sand (0.5 to 0.25 mm); fine sand (0.25 to 0.125 mm), very fine sand (0.125 to 0.063 mm); silt (0.063 to 0.004 mm); and clay (grain size <0.004 mm).
Photographs of the collected organisms were captured using a Canon EOS Sl3 camera with an EF-s 18-55 IS STM lens. Specimens were positioned on a black clipboard using a tape measure for scale reference. The photos documented key morphological characteristics for accurate identification of these individuals. All laboratory analyses were performed at Laboratório de Ciências Ambientais of Universidade Estadual do Norte Fluminense Darcy Ribeiro.
Results
Abiotic characterization of the recording sites
The environmental conditions of both beaches are summarized in Table 1. Physical–chemical parameters in surface water suggest saline waters in Piúma (salinity = 31.0 and conductivity = 47.6 mS cm−1), while indicating brackish waters in Guaxindiba (salinity = 23.0 and conductivity = 39.2 mS cm−1). Guaxindiba also shows lower concentrations of dissolved oxygen compared to Piúma (5.9 and 7.5 ppm, respectively), along with higher water temperatures (30.5 and 25.7°C, respectively). In contrast, abiotic conditions measured inside the galleries show an inverse pattern: Piúma had lower salinity and conductivity (19.7 and 31.7 mS cm−1, respectively) compared to Guaxindiba (23.5 and 36.8 mS cm−1, respectively). Dissolved oxygen concentrations inside the galleries were lower than that of surface water in both areas (4.9 and 2.2 ppm, respectively).
Table 1. Morphometric measurements and abiotic conditions for two adult male specimens of Audacallichirus mirim collected from Piúma and Guaxindiba
Measurements include total length (TL), cephalothorax length (CL), left cheliped length (LCL) and width (LCW), right cheliped length (RCL) and width (RCW), and total weight (TW). Abiotic conditions were measured at both the surface water and within the galleries, including temperature, pH, conductivity, salinity, and dissolved oxygen (DO) in both ppm and percentage.
The granulometric composition of the beaches was primarily composed of fine sand (approximately 31%) and very fine sand (approximately 41%) at Piúma Beach, with coarser fractions making up the remaining 28%. At Guaxindiba Beach, the composition included fine sand (approximately 57%) and very fine sand (approximately 20%), with coarser fractions constituting the remaining 23%.
Description of species characteristics and specimens
These collections represent the first record of this species in southern Espírito Santo and northern Rio de Janeiro, southeastern Brazil (Figures 2 and 3, respectively). Biometric measurements of the specimens are provided in Table 1.
Figure 2. Specimen of A. mirim from Piúma Beach, Espírito Santo state: (A, B), dorsal view and (C), telson, dorsal view (scale = 1.0 cm).
Figure 3. Specimen of A. mirim from Guaxindiba Beach, Rio de Janeiro state: (A, B), dorsal view and (C), telson, dorsal view (scale = 1.0 cm).
Taxonomy
Kingdom ANIMALIA
Phylum ARTHROPODA von Siebold, 1848
Subphylum CRUSTACEA Brünnich, 1772
Class MALACOSTRACA Latreille, 1802
Order DECAPODA Latreille, 1802
Suborder PLEOCYEMATA Burkenroad, 1963
Infraorder AXIIDEA de Saint Laurent, 1979
Family CALLICHIRIDAE Manning and Felder, 1991
Genus Audacallichirus Poore, Dworschak, Robles, Mantelatto & Felder, Reference Poore, Dworschak, Robles, Mantelatto and Felder2019
Species Audacallichirus mirim Rodrigues, 1971
Material Examined
Diagnosis was adapted from Hernáez et al. (Reference Hernáez, Pinheiro, Almeida Alves-Junior and Santana2022b). The carapace exhibits a small triangular rostrum along with two rounded anterolateral projections (Figures 2A and 3A). The ocular peduncles are contiguous, except for a separated blunt apical portion, which fails to reach the second article of the antennular peduncles. Notably, the antennular peduncle appears longer and stouter than the antennal peduncle, with the second article of the antennular peduncle slightly exceeding the fourth article of the antennal peduncle. The third merus of the maxilliped displays non-parallel distal and proximal margins, featuring a strong distal obliquity without projecting beyond the carpo-meral articulation. The male major cheliped merus is characterized by a prominent hook on the lower margin, while the fixed finger bears a small triangular tooth at the midpoint of the cutting edge. The dactylus exhibits a strong arcuate shape with a downwardly curved tip, bifid and longer than the fixed finger. Its cutting edge showcases a large bifid tooth proximally, otherwise remaining unarmed. The male second pleopod presents well-developed endopod and exopod. The telson is slightly broader than long, tapering distally, and emarginate posteriorly.
Discussion
The ghost shrimp Audacallichirus mirim constitutes one of 46 species of burrowing shrimp documented along the Brazilian coast (Hernáez et al., Reference Hernáez, Pinheiro, Almeida Alves-Junior and Santana2022b), although it is not always the most abundant. The number of Callichirus corruptus individuals captured on the beaches of Guaxindiba and Piúma was significantly higher (a 30:1 ratio) compared to the records of A. mirim on each beach. Despite its wide geographic distribution, spanning from the coast of Bahia to Rio Grande do Sul, A. mirim is often underrepresented in field collections. This discrepancy can be explained by several factors, including differences in habitat preference, niche partitioning, and abiotic filtering of species based on environmental conditions. For example, C. corruptus typically inhabits higher intertidal zones, which may make it more accessible during sampling. In contrast, A. mirim is more often associated with subtidal zones, estuaries, or tidal flats, making it more difficult to capture using the same sampling methods (Pezzuto, Reference Pezzuto1998).
The environmental conditions at Piúma and Guaxindiba beaches, where A. mirim was found, align with previous reports on its habitat. The known ranges for this species include temperatures from 12 to 27°C, salinity from 12 to 36, and preferred grain size composed by fine sands (median = 2.88Ø) (Pezzuto, Reference Pezzuto1998). These conditions were previously measured in the surf zone in southern Brazil and suggest that A. mirim may be better adapted to cooler environments (Pezzuto, Reference Pezzuto1998). Our recorded temperatures, ranging from 25.7 to 30.5°C, were measured in the swash zone and within the inhabited burrows of A. mirim, suggesting a higher temperature tolerance for the species in southeastern Brazil.
Although our salinity measurements, ranging from 19.7 to 31.0, were consistent with those reported in southern Brazil by Pezzuto (Reference Pezzuto1998), ocean salinity values were more prominent in the surface waters of Piúma, in contrast to the brackish surface waters observed at Guaxindiba. Thus, the species also appears to have wide tolerance limits for salinity variations, corroborating its occurrence in tidal flats. Therefore, the low number of A. mirim individuals captured in our study may reflect the natural rarity of this species in terms of abundance rather than local environmental filter. In addition, the low abundance may be linked to seascape features, including ocean currents that affect larval dispersal and recruitment patterns.
Nonetheless, this record is historically significant, providing evidence of a spatial overlap between A. mirim and C. corruptus, which has not been previously documented, even in states such as Bahia and São Paulo, where both species occur (Hernáez et al., Reference Hernáez, Pinheiro, Almeida Alves-Junior and Santana2022b). This overlap is especially intriguing and raises questions about subtle environmental similarities between the sampled beaches that may support both species. Such findings highlight the importance of understanding species-specific habitat preferences, which are crucial for future conservation efforts.
We acknowledge that our sampling efforts did not specifically target A. mirim, and thus it may have affected the species' representativeness. Thus, future studies on its distribution at a finer scale and its habitat are necessary for more efficient sampling. This could confirm its natural rarity and increase our knowledge of the species ecological role and population dynamics. This research will be essential for developing conservation strategies and ensuring the conservation of this potentially important fishery resource and its habitats.
Data
All relevant data are available in the paper. Additional data are available from the corresponding author on reasonable request.
Author contributions
K. A. F. and L. L. C. conceived the study. K. A. F., L. M. S. V., P. V. G., M. E. A. S. S., and L. L. C. performed the investigations. K. A. F., L. M. S. V., and L. L. C. performed the statistical analyses. K. A. F. wrote the manuscript. L. L. C. supervised the project and reviewed the draft manuscript. All authors reviewed and approved the manuscript.
Financial support
This research was supported by Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro – FAPERJ (K. A. F., Grant number E-26/210.238/2024; L. L. C., Grant number E-26/200.620/2022; and P. V. G., Grant number E-26/204.508/2021).
Competing interests
None.
