Larval development of the spider crab Menaethius monoceros (Latreille, 1825), (Crustacea: Decapoda: Brachyura: Epialtidae)

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Larval development of the spider crabMenaethius monoceros (Latreille,1825), (Crustacea: Decapoda:Brachyura: Epialtidae)Jessica Colavitea, William Santanaa & Gerhard Pohleb

a Pró-Reitoria de Pesquisa e Pós-Graduação, Universidade SagradoCoração – USC, Bauru, SP, Brazilb Atlantic Reference Centre, Huntsman Marine Science Centre, St.Andrews, New Brunswick, CanadaPublished online: 11 Jun 2014.

To cite this article: Jessica Colavite, William Santana & Gerhard Pohle (2014) Larval developmentof the spider crab Menaethius monoceros (Latreille, 1825), (Crustacea: Decapoda: Brachyura:Epialtidae), Journal of Natural History, 48:37-38, 2273-2292, DOI: 10.1080/00222933.2014.925596

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Larval development of the spider crab Menaethius monoceros(Latreille, 1825), (Crustacea: Decapoda: Brachyura: Epialtidae)

Jessica Colavitea, William Santanaa* and Gerhard Pohleb

aPró-Reitoria de Pesquisa e Pós-Graduação, Universidade Sagrado Coração – USC, Bauru, SP,Brazil; bAtlantic Reference Centre, Huntsman Marine Science Centre, St. Andrews,New Brunswick, Canada

(Received 11 December 2013; accepted 12 May 2014; first published online 11 June 2014)

The larval development of the spider crab Menaethius monoceros (Latreille, 1825)(Crustacea: Decapoda: Brachyura: Majoidea: Epialtinae) is described and illu-strated from laboratory-reared larvae. The development consisted of two zoealstages and one megalopa, following the typical pattern in Majoidea. The durationof the first zoeal stage was 4–11 days, the second zoea appearing 5–12 days and themegalopa 10–18 days after hatching. Both zoeal stages of Menaethius monoceroshave a distinct setation on the distal segment of the endopod of maxilliped II. Inthe megalopa only the setation of the exopod of the antennule is diagnostic amongEpialtinae. Comparative analysis revealed that some of the previous descriptionsare probably not those of Menaethius monoceros. Based on existing limited infor-mation no single morphological feature, or set of features, is apparent thatcharacterizes epialtine larvae.

Keywords: Majoidea; Epialtinae; larval morphology; ontogeny

Introduction

With about 15,000 valid species, Decapoda represents the most diverse order amongall crustaceans, including crabs, shrimps and lobsters (De Grave et al. 2009; Martinet al. 2009). Brachyura, commonly known as ‘true crabs’, comprises about 45% ofdecapods. Among the latter, the superfamily Majoidea is the most numerous, withapproximately 1000 species (De Grave et al. 2009). Members of this superfamily canbe found in all regions of the globe, mostly in tropical regions, with some speciesrestricted to temperate waters of the Pacific and Atlantic oceans.

Included among Majoidea are commercially very important species, such asChionoecetes opilio (Fabricius, 1788) and Maja brachydactyla Balss, 1922. In 2011,almost 206,000 tons of majoids were fished worldwide (FAO 2013). Numerousmajoid species are also of substantial ecological importance, particularly withincoral reef environments (Reed et al. 1982).

Recent classifications divide Majoidea into six families (Ng et al. 2008; De Graveet al. 2009; Ahyong et al. 2011). Epialtidae is the most speciose among these familiesand includes Menaethius monoceros (Latreille, 1825), a widely distributed speciesoccurring throughout the Indo-Pacific, the Tasman and Red Sea (Griffin andTranter 1986) and that has also been reported as an exotic species in theMediterranean (Öztürk 2010).

*Corresponding author. Email: [email protected]

Journal of Natural History, 2014Vol. 48, Nos. 37–38, 2273–2292, http://dx.doi.org/10.1080/00222933.2014.925596

© 2014 Taylor & Francis

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Menaethius monoceros is commonly found among macroalgae (e.g. Sargassum),algal banks in rock formations and sandy-muddy bottoms (Davison et al. 2008). Thisspecies has a wide geographical distribution living, in most cases, associated withalgal banks. The loss of these habitats, by either direct or indirect human action hasimpacted this species. In some localities M. monoceros is considered as ‘Vulnerable’according to the criteria of the International Union for the Conservation of Nature(IUCN), as is the case in Singapore (Davison et al. 2008). Thus, knowledge of itsearly life history is fundamental for the establishment of conservation parameters ofthe species within the areas they inhabit.

Within Epialtidae, larvae of the subfamily Epialtinae are poorly known. Amongthe 115 valid species, there is larval information for only 14 taxa. This includes someinformation on larvae of Menaethius monoceros by Gohar and Al-Kholy (1957) andTerada (1981). However, these previous descriptions are incomplete, inadequatelyillustrated with missing or small and poorly detailed figures that do not conform topresent-day standards (Clark et al. 1998) and that lack details on setal types (Pohleand Telford 1981) and meristics (including variability).

Larval descriptions are also fundamental for the identification of species withinthe plankton, an essential component in the trophic chain of the oceans.Furthermore, the use of larval data in phylogenetic analyses is growing, and hasproved to be useful to establish relationship hypotheses and evolutionary patternswithin several brachyuran groups (Pohle and Marques 2000; Santana et al. 2004;Clark 2009; Hultgren et al. 2009). Here we describe and illustrate in detail thecomplete larval development of Menaethius monoceros, with emphasis on the mor-phological features of Majoidea, and compare the morphology of M. monoceros withother Epialtinae genera.

Material and methods

Larval development and description

Specimens of Menaethius monoceros (Latreille, 1825) were collected on 24 July 2001off Heron Island, Queensland, Australia. Ovigerous specimens were held in anaquarium in a temperature-controlled room (24 ± 2°C) until hatching, whichoccurred at night. After hatching, 50 of the most active, positively phototactic larvaewere individualized into 100 ml acrylic jars containing 50 ml of filtered seawater. Theremaining larvae were kept in mass culture as additional specimens to be used formorphological description.

Newly hatched larvae were fed ad libitum with Artemia nauplii, rotifers andmicroalgae reared in the laboratory. Seawater was changed, and specimens wereinspected and fed daily. All acrylic jars were washed in fresh water and air-driedbefore re-use with fresh seawater the following day. Average salinity was 32. Anatural photoperiod was maintained (ffi12L:12D).

Whenever possible, a minimum of five specimens of each stage was dissected formorphological description. For slide preparations polyvinyl lactophenol was used asmounting medium with acid fuchsin and/or chlorazol black. The description of setaefollows Pohle and Telford (1981), but here includes only analysis by light microscopy(LM), using an Olympus BH-2 (Shinjuku, Tokyo, Japan) and a Zeiss Axioskop II FSPlus (Oberkochen, Germany), both equipped with camera lucida. Some of the setae

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designated as plumose herein may be plumodenticulate due to the lower resolutionlimits of LM as compared to scanning electron microscopy (SEM). Descriptionguidelines of Clark et al. (1998) were generally followed. Taxonomic rankings followNg et al. (2008) in which some majid subfamilies were raised to the family level andincluded within Majoidea.

Specimens of larval stages and a spent female crab are deposited at the Museu deZoologia da Universidade de São Paulo (MZUSP), São Paulo State, Brazil (MZUSP21735; 21736).

Results

Larval development and description

Larval development of Menaethius monoceros consists of two zoeal stages and onemegalopa. The duration of the first zoeal stage was 4–11 days, the second zoeaappearing 5–12 days and the megalopa 10–18 days after hatching. Only morpholo-gical changes are described for the second zoea.

Infraorder BRACHYURA Linnaeus, 1758Superfamily MAJOIDEA Samouelle, 1819Family EPIALTIDAE MacLeay, 1838

Subfamily EPIALTINAE MacLeay, 1838Menaethius monoceros Latreille, 1825

First zoea (Figure 1)

Carapace (Figure 1A). Without dorsal and lateral spines, rostral spine greatly dimin-ished. Ventral margin with densely plumose ‘anterior seta’ (Clark et al. 1998) poster-ior to scaphognathite notch, followed by 2–4 smaller plumose setae; carapaceotherwise without setae. Eyes sessile. Frontal area bearing a dorsal organ (sensuMartin and Laverack 1992; Lerosey-Aubrill and Meyer 2013).

Antennule (Figure 1B). Unsegmented, smooth, conical. Terminally bearing 2 long, 2shorter aesthetascs, and 1–2 short simple setae.

Antenna (Figure 1C). Biramous, protopod long and pointed, bearing 2 rows of sharpspinules; endopod bud present; one-segmented exopod slightly longer than protopodwith long spinulated distal process; pair of setae about one third from tip, oneserrulate and one simple.

Mandible (Figure 1D). With medial toothed molar process and enlarged lateralincisor processes; marginal teeth between molar and incisor processes. Palp absent.

Maxillule (Figure 1E). Coxal endite bearing 7 setae, 4 graded plumodenticulateterminally, 3 plumodenticulate subterminally. Basial endite with 4 terminal plumo-denticulate cuspidate setae and 3 subterminal plumodenticulate setae. Two-segmen-ted endopod, proximal segment without seta, distal segment with 5 plumodenticulatesetae, 1 subapical and 4 terminal. Exopod seta absent.

Journal of Natural History 2275

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Figure 1. First zoea of Menaethius monoceros (Latreille, 1825). (A) lateral view and magnifiedventrolateral carapace margin (maxilliped natatory setae shown truncated); (B) antennule; (C)antenna (endopod bud stippled); (D) right mandible; (E) maxillule, with enlargement of coxaland basial endites; (F) maxilla, with enlargement of coxal and basial endites; (G) maxilliped I,with enlargement of distal endopod segment; (H) maxilliped II; (I) dorsal view of abdomen andtelson. Scale bars = 0.1 mm.


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Maxilla (Figure 1F). Coxal endite bilobed, proximal lobe with 4–5 setae, 3–4plumose and 1 plumodenticulate; distal lobe with 3–4 setae, 1–2 plumose and 2plumodenticulate. Basial endite bilobed, proximal and distal lobes with 5 and 4plumodenticulate setae, respectively. Microtrichia present on both endites.Unsegmented endopod unilobed, with 5 plumodenticulate setae, 3 apical and 2subapical; microtrichia on distal margin. Scaphognathite marginally with 9–11 den-sely plumose setae, including distal process.

Maxilliped I (Figure 1A, G). Coxa with plumodenticulate seta. Basis with 9 plumo-denticulate setae arranged 2 + 2 + 2 + 3. Endopod 5-segmented with 3, 2, 1, 2, 4plumodenticulate setae and an accessory spine on the distal segment. Incompletelybisegmented exopod with 4 terminal plumose natatory setae.

Maxilliped II (Figure 1A, H). Coxa without seta. Basis with 3 plumodenticulatesetae. Endopod three-segmented, with 0, 1, 4 plumodenticulate setae, distal segmentwith 2 subapical, 2 apical setae. Incompletely bisegmented exopod with 4 terminalplumose natatory setae.

Maxilliped III (Figure 1A). Present as a small undifferentiated bud.

Pereiopods (Figure 1A). Present as small buds, chela indistinct.

Pleon (Figure 1A, I). Five somites. Somite 1 with pair of middorsal long simple setae,somites 2–5 each with pair of shorter posteromedial simple setae. Posterolaterally,somite 2 with blunt process, somites 3–5 with short lateral projections; somite 2 withpair of dorsolateral processes. Pleopod buds rudimentary.

Telson (Figure 1I). Bifurcated, without median notch, three pairs of plumodenticu-late setae on inner margin; each furcal shaft proximally bearing lateral spine, furcalshafts and spines covered in rows of spinules to just below tips.

Second zoea (Figure 2)

Carapace (Figure 2A). Eyes mobile. Ventral margin with densely plumose anteriorseta followed by 3–4 plumose setae; pair of small plumodenticulate setae dorsally.

Antennule (Figure 2B). With 6–7 long aesthetascs and a short simple seta, endopodbud present.

Antenna (Figure 2C). Endopod bud enlarged to just beyond middle of protopodite.

Mandible (Figure 2D). Palp bud present.

Maxillule (Figure 2E). Basial endite with 9–10 setae, additional graded plumodenti-culate seta terminally, additional plumodenticulate setae subterminally; optional verysmall plumodenticulate seta on proximal margin; exopod pappose seta present.


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Figure 2. Second zoea of Menaethius monoceros (Latreille, 1825). (A) lateral view and magni-fied ventrolateral carapace margin (maxilliped natatory setae shown truncated); (B) antennule;(C) antenna; (D) right mandible; (E) maxillule, with enlargement of coxal and basial endites;(F) maxilla, with enlargement of coxal and basial endites; (G) chela and pereopods; (H) dorsalview of abdomen and telson. Scale bars = 0.1 mm.


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Maxilla (Figure 2F). Basial endite with 5 plumodenticulate setae on proximal lobeand distal lobe; Scaphognathite with 19–21 marginal plumose setae.

Maxilliped I (Figure 2A). Exopod with 6 plumose natatory setae.

Maxilliped II (Figure 2A). Exopod with 6 plumose natatory setae.

Maxilliped III (Figure 2A,G). Exo-, endo- and epipod buds distinct.

Pereiopods (Figures 2A,H). Longer, chela apparent.

Pleon (Figures 2A, I). Additional sixth somite. Posterolaterally, somites 1 and 6 withblunt processes, somites 2–5 with enlarged lateral projections; somite 1 with threemiddorsal long simple setae. Pair of unsegmented biramous pleopods on somites 2–5,endopods very small.

Megalopa (Figures 3 and 4)

Carapace (Figures 3A, B). Longer than wide, subrectangular; rostral spine veryshort, ventrally deflected; hepatic region projected, forming 1 knob-like lateral expan-sion, gastric region well developed, divided in 2 regions, protogastric and metagastric;protogastric region swollen bearing the dorsal organ medially; branchial, cardiac andintestinal regions well defined, inflated. Posterior margin with 10 simple setae, surfacecovered mostly with simple setae as shown.

Antennule (Figure 3C). Three-segmented peduncle, proximal segment without setae,middle and distal segments with one simple seta each; endopod unsegmented with 1subterminal and 2 terminal long simple setae. Four-segmented exopod, first segmentwithout seta, second segment with 6 aesthetascs and simple seta, third segment with 4aesthetascs, distal segment with aesthetasc-like subapical seta.

Antenna (Figure 3D). Segments 1–7, progressing proximally to distally, each with 1,2, 3, 0, 0, 4, 4 simple setae, respectively. Basal segment with distinct exopod process.

Mandibles (Figure 3E). Asymmetrical, scoop-shaped process with cutting edge and smallacute tooth; two-segmented palp bearing 5 plumodenticulate setae on the distal segment.

Maxillule (Figure 3F). Coxal endite with 5 graded plumodenticulate setae apically, 3plumodenticulate setae, and a plumose seta subterminally. Basial endite with 17 setae,7 plumodenticulate cuspidate terminally, 8 plumodenticulate subterminally, 2 plu-mose setae on proximal margin. Epipod plumodenticulate seta present; two-segmen-ted endopod lacking outgrowths.

Maxilla (Figure 3G). Coxal endite bilobed; proximal lobe with 6 setae, 5 plumosesetae and 1 plumodenticulate seta; distal lobe bearing 2 plumose setae. Basial enditewith 5 and 6 plumodenticulate setae on proximal and distal lobes, respectively.Endopod reduced, with microtrichia on distal margin, without setae.Scaphognathite with 28–31 marginal plumose setae; blade with 3 simple setae.


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Figure 3. Megalopa of Menaethius monoceros (Latreille, 1825). (A) lateral view; (B) dorsalview; (C) antennule, with aesthetascs shown truncated; (D) antenna; (E), left mandible, withenlargement of distal palp segment; (F) maxillule; (G) maxilla. Scale bars = 0.1 mm.


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Figure 4. Megalopa of Menaethius monoceros (Latreille, 1825). (A) maxilliped I; (B) maxillipedII, with enlargement of distal endopod segments; (C) maxilliped III; (D) pleopods 1–4 anduropod (natatory setae shown truncated, without setules), distal setae shown truncated; (E)cheliped and pereiopods; (F) sternum; (G) dorsal view of abdomen and telson. Scalebars = 0.1 mm.


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Maxilliped I (Figure 4A). Coxa with 6 plumodenticulate setae, basis bearing 10–11plumodenticulate setae; endopod without setae; exopod with pappose seta distally onproximal segment, 4 plumose setae on distal segment; epipod with 4 plumodenticulatesetae, 1 proximal, 3 distal.

Maxilliped II (Figure 4B). Coxa and basis not clearly differentiated; four endopodsegments proximally to distally with 0, 1, 3 and 6 plumodenticulate setae, respec-tively; exopod with naked proximal segment and 4 plumose setae on distal segment;epipod not present on examined specimens.

Maxilliped III (Figure 4C). Coxa with 1 + 4 plumodenticulate setae, basis fused toischium, endopod proximally to distally with 10–11 + 1, 5–6 + 3, 4 + 2, 4 and 4plumodenticulate setae; ischium with protuberances indicative of crista dentata;bisegmented exopod, naked proximal segment, distal segment with 4 plumose setaeapically; epipod with short plumodenticulate seta proximally, 3 long plumodenticu-late setae distally.

Pereiopods (Figure 4D). Cheliped with mostly simple setae; pereiopods 2–5 mostlywith simple setae; basischial segments without spines; coxa of pereiopod 2 withprominent spine; dactyls of pereiopods 2–5 with rows of spinules as shown; 1–2serrulate setae near tip of dactyls on ventral margin.

Sternum (Figure 4E). Segments 1–3 completely fused into single plate with bell-shaped anterior margin, without setae; segment 4 with 2 pairs of simple setae;segment 5 with 1 pair of simple setae; subsequent segments without setae.

Pleon (Figure 4F). Somites 1–5 proximally to distally with 4, 8, 6, 6, 6 simple setaedorsally and laterally, sixth somite with 2 simple setae.

Pleopods (Figure 4G). Four pairs of pleopods, exopods each with 11, 11, 10, 8plumose natatory setae, respectively; endopod with 2 cincinnuli each. Uropodreduced, segments fused, with 5 plumose setae distally, endopod absent.

Telson (Figure 4F). Rounded posteriorly, bearing a pair of simple dorsal setae.

Discussion

Currently Majoidea encompasses six families comprising Majidae Samoulle, 1819;Epialtidae Macleay, 1838; Inachidae Macleay, 1838; Inachoididae Dana, 1851;Oregoniidae Garth, 1958 and Hymenosomatidae Macleay, 1838 (Ng et al. 2008;De Grave et al. 2009; Ahyong et al. 2011), the inclusion of the latter still beingdebatable. In terms of larvae, almost all majoids are characterized by two zoeal stagesand a megalopa, with the exception of Hymenosomatidae. However, the categoriza-tion and unambiguous characterization of majoid groups and the assignment ofgenera and species to such groups is still problematic. The exception is Oregoniidaefor which larval morphology and genetic evidence indicate this to be a basal mono-phyletic group (Hultgren et al. 2009) among Majoidea. With the inclusion of theformer family Pisidae Dana, 1851 as a subfamily of Epialtidae (Ng et al. 2008), this


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group composed of four subfamilies is probably the most heterogeneous amongMajoidea. The separation among these subfamilies is unclear in several cases. Theplacement of various genera and species also needs revision based on adult morphol-ogy, as is the case for the clearly closely related genera Pugettia Dana, 1851 andRochinia A. Milne-Edwards, 1875, that are currently distantly classified as Epialtinaeand Pisinae, respectively (see Ng et al. 2008). Similar challenges exist based onevidence from larval morphology. For example, Kornienko and Korn (2007) con-cluded that the zoea of Pugettia quadridens (De Haan, 1839) and Pisoides bidentatus(A. Milne-Edwards, 1873), presently assigned to Epilatinae and Pisinae, respectively,are nearly identical, while the larvae of two species of Pisoides H. Milne Edwards andLucas, 1843, P. bidentatus and P. edwardsii (Bell, 1835), differ in numerous char-acters. Also, adult morphology indicates that Huenia proteus (De Haan, 1839) is ajunior synonym of Huenia heraldica (De Haan, 1837) (see Holthuis 1987); thus wetreated the larval description of H. proteus as H. heraldica. Goniopugettia sagamiensis(Gordon, 1931) was transferred from Epialtinae to Pisinae (Ng et al. 2008), thereforethis species was not included in our comparisons. Larvae of Pugettia quadridens havebeen described by a number of authors (Table 1), but here we related our results tothose of Kornienko and Korn (2004), as this is the most complete and detaileddescription for that taxon. In the present study we compared the larval morphologyof 16 Epialtinae species with partial or complete descriptions (Table 1).

Identification and affinities of Menaethius monoceros larvae

Disregarding data of Gohar and Al-Kholy (1957) on M. monoceros (see below),characters of the first zoeal stage that are shared with other Epialtinae include thesetal meristics of the coxa and basis of the maxillule (except in Acanthonyx limbatusA. Milne-Edwards, 1862, Epialtus brasiliensis Dana, 1852 and E. bituberculatus H.Milne Edwards, 1834), the proximal lobe of the basis of the maxilla and the endopodof maxilliped II (Table 2). In the second zoea only the endopod of maxilliped II ischaracterized by the same number of setae in all the studied species (Table 3).Meristically there appear to be no consistent similarities between all species at themegalopa stage (Tables 3 and 4). However, some appendages are similar among mostspecies, including the endopod of the antennule bearing three setae (except in Epialtusbituberculatus, Pugettia intermedia Sakai, 1938 and P. marissinica Takeda andMiyake, 1972), as well as the setation on the endopod and exopod of maxilliped II(except in E. bituberculatus, P. marissinica and Taliepus dentatus (H. MilneEdwards, 1834)) (Tables 3 and 4).

Our results indicate that Menaethius monoceros is easily distinguished from otherEpialtinae in terms of larvae. Both zoeal stages present a distinct setation on theendopod of maxilliped I (Tables 1 and 2). The distinct spine in the distal segment ofthe endopod of the first maxilliped is unusual, especially considering the presence ofsetules on that structure. However, this spine is shared with the epialtine Hueniaheraldica in zoea II, according to Terada (1981). This feature is also found in othermajoids, such as the mithracine Macrocoeloma diplacanthum (Stimpson, 1860) (cf.Marques et al. 2003). In the megalopa only the exopod of the antennule is diagnosticamong Epialtinae (Table 4).

Epialtus H. Milne Edwards, 1834 seems to form a morphologically coherentgroup sharing several distinct similarities in each larval stage. This group is easily


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recognizable by the setal formulae on the endopod of the maxillule in zoea I; theunilobed coxa of the maxilla in zoeas I, II and the megalopa; and in the megalopabased on setal meristics of the coxa and basis of the maxilla and first maxilliped(Tables 2, 3 and 4). In contrast, other epialtine groups are difficult to identify due togreater variability among species either within (e.g. Acanthonyx Latreille, 1828 andPugettia) or between genera (Tables 2, 3 and 4).

Some intergeneric similarities are stage dependent. In zoea I Menaethius mono-ceros resembles Leucippa pentagona H. Milne Edwards, 1834, Pugettia quadridensand Taliepus dentatus, sharing meristics of the ventral margin of the carapace,antennule, coxa and basis of the maxillule, basis of the maxilla and first maxilliped

Table 1. Species of Epialtinae with known larval descriptions indicating source and stagesdescribed.

Species Authors Stages described

Acanthonyx limbatus A. Milne-Edwards, 1862

Ghory and Siddiqui (2009); Kakati andSankolli (1975)

ZI, ZII; ZI, ZII,M

A. lunulatus (Risso, 1816) Guerao and Abelló (1996) ZI, ZII, MA. scutiformis (Dana, 1851)described as A. petiverii H.Milne Edwards, 1834*

Hiyodo et al. (1994) ZI, ZII, M

Epialtus bituberculatus H. MilneEdwards, 1834

Negreiros-Fransozo and Fransozo(1991)

ZI, ZII, M

E. brasiliensis Dana, 1852 Negreiros-Fransozo and Fransozo(2001)

ZI, ZII, M

E. dilatatus A. Milne-Edwards, 1878

Yang (1968) ZI, ZII, M, CI

Huenia heraldica (De Haan,1837) described as H. proteus(De Haan, 1839)†

Aikawa (1937); Kurata (1969); Terada(1981)

ZI; ZI; ZI, ZII

Leucippa pentagona H. MilneEdwards, 1834

Pohle and Marques (2003) ZI, ZII, M

Menaethius monoceros (Latreille,1825)

Gohar and Al-Kholy (1957); Terada(1981)

PZ, ZI, ZII, M;ZI, ZII

Pugettia gracilis Dana, 1851 Oh and Ko (2007) ZIP. incisa (De Haan, 1839) Kurata (1969); Terada (1981) ZI, M; ZI, ZIIP. intermedia Sakai, 1938 Terada (1981); Ko and Hwang (1997);

Ko (1998)ZI, ZII; M; ZI,ZII

P. marissinica Takeda andMiyake, 1972

Ko and Hwang (1997); Ko (1998) ZI, ZII; M

P. quadridens (De Haan, 1839) Aikawa (1929); Kurata (1969); Iwata(1970); Terada (1981); Ko andHwang (1997); Ko (1998); Kornienkoand Korn (2004)

ZI; ZI; ZI; ZI,ZII; M; ZI; PZ,ZI, ZII, M

P. similis Rathbun, 1832 Terada (1981) ZI, ZIITaliepus dentatus (H. MilneEdwards, 1834)

Fagetti and Campodonico (1971) ZI, ZII, M

Note: *vide Pohle and Marques (2003); †vide Holthuis (1987); PZ: prezoea; ZI: zoea I; ZII:zoea II; M: megalopa; CI: first juvenile.


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Tab

le2.

Com

parisonof

larval

characters

ofthefirstzoealstag

eforspeciesof

thesubfam

ilyEpialtina

e.

Carap

ace

ventral

Max

illule

Max

illa

Max

illiped

IMax

illiped

II

Species

margin

Antennu

leCox

aBasis

End

opod

Cox

aBasis

End

opod

Basis

End

opod

End

opod

Acantho

nyxlim

batus

112+2

68

73+3

5+5

52+2+3+3

3,2,1,2,1+4

0,1,4

A.lunu

latus

73+1

77

0,4

5+3

5+4

52+2+3+3

3,2,1,2,1+4

0,1,4

A.scutiformisas

A.petiverii

ND

3+1

73+4

0.4

5+3

5+4

52+2+3+3*

3,2,1,2,5

0,1,4

Epialtus

bituberculatus

73+1

6-7

80,2+4

64+5-6

62+2+3+3

3,2,1,2,5-6

0,1,4

E.brasiliensis

4-5

3+1

47-8

0,2+4

55+3

53+1+2+3*

3,2,1,2,4-5

0,1,4

E.dilatatus

92+1

77

0,2+4

65+4

52+2+2+3

3,2,1,2,1+4

0,1,4

Hueniaheraldicaas

H.proteus

ND

ND

ND

ND

0,1+4

5+4*

5+4*

4*2+2+2+3

3,2,1,2,1+4

0,1,4

Leucipp

apentag

ona

54+2

77

1.4

4+4

5+4

52+2+3+3

3,2,1,2,4

0,1,4

Pug

ettiagracilis

73+2

77

1.4

4+4

5+4

32+2+2+3

3,2,1,2,5

0,1,4

P.incisa

ND

ND

ND

ND

ND

4+4*

5+4*

3*ND

ND

ND

P.interm

edia

54+2

77

1.4

4+4

5+4

42+2+2+3

3,2,1,2,1+4

0,1,4

P.marissinica

53+2

77

1.4

4+4

5+4

42+2+2+3

3,2,1,2,

1+4

0,1,4

P.qu

adridens

54+2

77

1.4

4+4

5+4

42+2+2+3

3,2,1,2,1+4

0,1,4

P.similis

ND

5+1*

7*7*

1,4*

ND

ND

ND

2+2+2+3

3,2,1,2

0,1,4*

Taliepu

sdentatus

44+2

77

1.5

5+4

5+4

42+2+2+3

3,2,1,2,4-5

0,1,4

Menaethius

mon

oceros

(Terad

a,19

81)

ND

4+1*

7*7*

0,1+4*

ND

ND

ND

2+2+2+3*

3,2,1,2,1+4*

ND

M.mon

oceros

(Goh

aran

dAl-

Kho

ly,19

57)

ND

ND

77

0,1+4

ND

ND

52+2+2+3

3,2,1,2,1+4

0,1,4

M.mon

oceros

(present

stud

y)1+3-4

4+1-2

6-7

70,1+4

4-5+4

5+4

52+2+2+3

3,2,1,2,SP

+4

0,1,4

Note:

SP:spine;

ND:no

tdescribed;

*observa

tion

from

figu

re.


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Tab

le3.

Com

parisonof

larval

characters

ofthesecond

zoealstag

eforspeciesof

thesubfam

ilyEpialtina

e.

Carap

ace

ventral

Max

illule

Max

illa

Max

illiped

IMax

illiped

II

Species

margin

Antennu

leCox

aBasis

End

opod

Cox

aBasis

End

opod

Scap

h.Basis

End

opod

Basis

End

opod

Acantho

nyxlim

batus

166+1

79

1,2+4

4+4

4+6

528

2+2+3+3

3,2,1,2,1+4

30,1,4

A.lunu

latus

96+2

810

0,4

5+3

5+5

522

2+2+3+3

3,2,1,2,1+4

20,1,4

A.scutiformisas

A.

petiverii

ND

6+2

710

0.4

5+3

5+4

522

2+2+3+3*

3,2,1,2,5

30,1,4

Epialtus

bituberculatus

95+1

8+2

111,2+4

65+5

5-6

20-21

2+2+3+3*

3,2,1,2,5

20,1,4

E.brasiliensis

6-7

7+1

47-8

0.6

63-4+3-

46

19-20

3+2+2+2*

3,2,1,2,5

40,1,4

E.dilatatus

ND

67

95

65+5*

522

AP

2+2+2+3

3,2,1,2,1+4

20,1,4

Hueniaheraldicaas

H.proteus

ND

7*ND

ND

0,1+4

ND

ND

4ND

2+2+2+3*

3,2,1,2,

SP+4*

ND

ND

Leucipp

apentag

ona

6-8

8-9+1-2

810

1,4

4+4

5+5

517

-20

2+2+3+3

3,2,1,2,4

30,1,4

Pug

ettiaincisa

ND

5+2*

ND

ND

ND

4+4*

5+5*

3*19

*ND

ND

ND

ND

P.interm

edia

77+1

710

1,4

4+4

5+5

418

2+2+2+3

3,2,1,2,1+4

30,1,4

P.marissinica

76+1

710

1,4

4+4

5+5

420

2+2+2+3

3,2,1,2,1+4

30,1,4

P.qu

adridens

76+2

710

1,4

4+4

5+5

420

2+2+2+3

3,2,1,2,1+4

30,1,4

P.similis

ND

5+1*

ND

ND

ND

ND

ND

4ND

ND

ND

ND

ND

Taliepu

sdentatus

46

610

1,5*

5+3

5+5

4*20

AP

2+2+2+3*

3,2,1,2,1+4*

30,1,4

Menaethius

mon

oceros

(Terad

a,19

81)

ND

5+1*

ND

ND

ND

4+5*

5+5*

5*18

*2+2+2+3

3,2,1,2,SP

+4

3*0,1,4*

M.m

onoceros

(Goh

aran

dAl-K

holy,1957)

ND

43

80,1+3

3+4

5+4

520

-25

ND

1,1,0,0,6

ND

2

M.mon

oceros

(present

stud

y)4-5

6-7+1

79-10

0,1+4

4+5

5+5

519

-21

2+2+2+3

3,2,1,2,SP

+4

30,1,4

Note:

AP:ap

prox

imate;

SP:spine;

ND:no

tdescribed;

scap

h.:scap

hogn

athite;*o

bserva

tion

from

figu

re.


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Tab

le4.

Com

parisonof

larval

characters

ofthemegalop

astag

eforspeciesof

thesubfam

ilyEpialtina

e.

Antennu

leMaxillule

Maxilla

Maxilliped

IMaxilliped

IIAbd

omen

Pleop

ods

Species

Carap

ace

End

opod

Exo

pod

Antenna

Cox

aBasis

End

opod

Cox

aBasis

End

opod

Scap

h.Cox

aBasis

Exo

pod

End

opod

End

opod

Exo

pod

Setae

Somites

12

34

Acanthonyx

lunulatus

Nospines

30,8+1,4,1

0,2,2,0,0,4,4

817

06+3

6+6

136

+2

49

1,4

00,1,3,6

0,4

2,8,8,8,6,2

612

1212

10

A.scutiformisas

A.petiverii

Nospines

30,9+1,3,1

0,1,1,0,0,3,4*

917

1+1

7+3

6+7

045-48

710

1,4

00,1,3,6

0,4

ND

612

1211

8

Epialtus

bituberculatus

Nospines

40,6+1,6,2

0,1,1,0,0,0,4

711

06

100

32+2

36

1,2

0.6

0,1,3,5

0,4

ND

610

1010

8

E.brasiliensis

Nospines

30,7+1,5,1+2

0,2,3,0,0,4,3

813

07

90

383

81,2

00,1,3,6

0,4

ND

612

12-1111-10

8-9

E.dilatatus

Nospines

30,6+1,4,1*

1,2,3,0,0,3,4

816

07

100

28-31

57*

1,4

00,1,3,5

0,4

6,8,6,8,8,2

612

1111

9

Leucippapentagona

Nospines

30,10-11+1,4+11,2,2,0,0,4,4

1017-18

2-3

6+3

6-7+6

033-37

710-11

1,4-6

00,1,3,6

0,4-6

2,8,8,8,8,2

611

12-11

119

Pugettiainterm

edia

Nospines

20,8+1,4,1

0,2,3,0,0,4,4

1016

1+2

6+3*

7+6*

035

611

1,4

00,1,3,6

0,4

ND

5ND

ND

ND

ND

P.marissinica

Nospines

30,8+1,4+1

0,2,3,0,0,4,4

1016

1+4

6+4*

7+6*

342

714

1,5

1+4

0,1,4,6

0,6

ND

6ND

ND

ND

ND

P.quadridens

Nospines

30,8+1,4+1-2

1,2,3,0,0,4,4

916-17

1+2

7+3*

7+7*

0-4

36-39

7-8

10-11

1,4-5

00,1,3,6

0,4

8,5,5,4,4,2

612

1110

9

Taliepusdentatus

Nospines

3*0,11

+1,4,3*

1,2,3,0,0,4,3

1017

AP

37+3

6+6

240*

612

AP

1,4

20,1,3,6

0,5

4,2,2,2,0,0*

613

12-11

1210

Menaethius

monoceros

(Goh

aran

dAl-

Kho

ly,1957

)

Dorsalspine

25

ND

77

03+5

3+2

0ND

411-15

30

0,0,0,8

0,3

ND

56

12-11

64*

M.monoceros

(present

stud

y)

Nospines

30,6,4+1,1

1,2,3,0,0,4,4

917

06+2

5+6

028-31

49

1,4

00,1,3,6

0,4

2,8,8,8,6,2

612

1212

10

Note:

AP:ap

prox

imately;

ND:no

tdescribed;

scap

h.:scap

hogn

athite;*o

bservation

from

figu

re.

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(Table 2). In the second zoeal stage M. monoceros shares several characters withPugettia intermedia, P. marissinica, and T. dentatus (Table 3). Both Pugettia specieshave the same number of setae on the antennule, coxa and basis of maxillule, basis ofmaxilla and maxilliped I, and maxilliped II. Zoea II of Taliepus dentatus shares withM. monoceros the setal meristics of the ventral margin of the carapace, basis ofmaxillule, maxilla and first maxilliped, and the basis and endopod of the secondmaxilliped (Table 3). In the megalopa M. monoceros is most similar to Pugettiaquadridens, followed by Leucippa pentagona. Both species share with M. monocerosthe number of setae on the endopod of the antennule, basis of maxillule, the absenceof setae on the endopod of the maxilla, basis and exopod of maxilliped I, maxillipedII, and pleopod II (Table 4). The megalopa of M. monoceros also shares the samenumber of setae on the coxa of the maxillule with Pugettia quadridens. With T.dentatus it shares several other characteristics including the setation of the endopodof the antennule, basis of the maxillule, coxa and exopod of maxilliped I, endopod ofmaxilliped II, and pleopod II (Table 4). However, comparisons are impaired by thenumber of incomplete descriptions of appendages and stages for a number of taxa,especially Huenia heraldica, Pugettia similis Rathbun, 1932, and P. incisa (De Haan,1839) (Tables 2 and 3). Therefore these comments can only be considered preliminaryconclusions in need of validation.

Comparison with previous descriptions

Menaethius monoceros was previously described by Gohar and Al-Kholy (1957) andTerada (1981); Terada (1981) did not describe the megalopal stage while Gohar andAl-Kholy (1957) described the prezoea, zoeal stages and the megalopa. These pre-vious studies not only lack morphological details but are very discrepant, withdifferences in setal types, number of setae and even gross morphology being found.

Gohar and Al-Kholy (1957) did not describe a number of structures, including thecarapace, antennule, and coxa and basis of the maxilla for zoea I; the setation of thecarapace and basis of maxillipeds I and II (Table 3) for zoea II; and the setation ofthe antenna, scaphognatite of the maxilla and abdomen for the megalopa (Table 4).Terada (1981) did not describe the setation of the carapace, maxilla, and maxilliped IIfor zoea I (Table 2), and the carapace and maxillule of zoea II (Table 3).

A comparison of described structures revealed that the most substantial differ-ences exist between the results of Gohar and Al-Kholy (1957) compared to findings ofTerada (1981) and the present study. These include differences in the setal formulas ofthe endopod of maxilliped I in zoea I, as well as for the antennules, maxillule,maxilla, and first and second maxillipeds for zoea II (Tables 2 and 3). However,most striking are gross morphological differences, Gohar and Al-Kholy (1957)describing a megalopa with five abdominal somites and a dorsal spine on thecarapace, in contrast to six abdominal somites and no dorsal spine in the presentstudy (Table 4). Therefore, while some consideration has to be given to possiblenatural morphological variation, the overall conclusion is that these differencesindicate that larvae described by Gohar and Al-Kholy (1957) most likely do notrepresent Menaethius monoceros.

In comparison, the results of Terada (1981) are much more in line with thepresent study. Our findings corroborate Terada’s in the setation of the antennule,maxillule, and basis of the first maxilliped in zoea I (Table 2). In the second zoeal


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stage we found similarities in the number of setae of the maxilla (except in thescaphognatite) and maxilliped II (Table 3). Some of the morphological differencesfound may be due to intraspecific variation. However, it is also possible that thesedifferences may be errors related to problems in specimen preparation or observation.

Acknowledgements

We thank Dr Fernando Portella de Luna Marques, University of São Paulo (USP), SãoPaulo – SP, Brazil, for collecting the female and laboratory rearing of larvae of M. monoceros.We also thank Dr Antônio L. Castilho, Dr Maria Lúcia Negreiros-Fransozo and Dr AdilsonFransozo, Núcleo de Estudos em Biologia, Ecologia e Cultivo de Crustáceos (NEBECC),Botucatu – SP, Brazil, for providing optical resources and working space. JC thanks DrRodney K. de Azevedo, Universidade Sagrado Coração (USC), Bauru – SP, for the help inslide preparations. JC and WS thank USC for supporting studies on the systematics of decapodcrustaceans.

FundingThis work was supported by the Fundação de Amparo à Pesquisa do Estado de São Paulo –

FAPESP [JP 99/10407-1, 99/08256-5, 2012/20564-3 and 2013/01201-0].

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Documents

Larval development of the spider crab Menaethius monoceros (Latreille, 1825), (Crustacea: Decapoda: Brachyura: Epialtidae)