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Accepted by J. Goy: 19 Nov. 2015; published: 18 Jan. 2016
ZOOTAXA
ISSN 1175-5326 (print edition)
ISSN
1175-5334
(online edition)
Copyright © 2016 Magnolia Press
Zootaxa 4066 (4): 399
–
420
http://www.mapress.com/j/zt/
Article
399
http://doi.org/10.11646/zootaxa.4066.4.3
http://zoobank.org/urn:lsid:zoobank.org:pub:E2065133-FC5B-4104-9A67-EFEE0BA3D004
Complete larval development of Thor amboinensis (De Man, 1888)
(Decapoda: Thoridae) described from laboratory-reared material
and identified by DNA barcoding
CÁTIA BARTILOTTI
1,3
, JOANA SALABERT
2
& ANTONINA DOS SANTOS
1
1
Instituto Português do Mar e da Atmosfera (IPMA), Avenida de Brasília, s/n, 1449-006, Lisboa, Portugal
2
Rua dos Cedros, nº 11, 4100-159 Porto, Portugal
3
Corresponding autor. E-mail: catia_bartilotti@hotmail.com
Abstract
Of the 12 species of Thor described until present date, only three (25%) have their complete larval development known.
Present work describes the complete larval development of Thor amboinensis, based on laboratory-reared material. The
spent females were identified through the analysis of the partial sequences of the mitochondrial DNA barcode, also used
for the reconstruction of the phylogenetic relationships within the recently resurrected and recognized family Thoridae
Kingsley, 1879. Eight zoeal stages and one decapodid complete this species larval development. In the genus Thor, the
number of zoeal stages varies greatly from two (T. dobkini) to eight (T. amboinensis and T. floridanus). The larvae of T.
ambionensis and T. floridanus are readily distinguished from each other by the ornamentation of the ventral margin of the
carapace and the pereiopods development. The first zoeal stage of T. amboinensis described by Yang & Okuno (2004) and
the one described in present study are very similar. A brief discussion on the morphological characters and on the number
of zoeal stages of the genus, as well as of the previous larval descriptions is made. The phylogenetic analysis suggest cryp-
tic speciation for geographical separated populations of T. amboinensis, paraphyly of the genus Eualus, and the reassign-
ment of E. cranchii to a different genus.
Key words: Hippolytidae, Thoridae, Thor, DNA barcode, zoeal stages, decapodid, larval morphology
Introduction
In recent years, the increase of aquarium trade had a great impact on decapod populations. Amongst the more
commercialized shrimp genera are Lysmata Risso, 1816, Periclimenes O.G. Costa, 1844a, Stenopus Latreille, 1819
and Thor Kingsley, 1878a (e.g. Rhyne & Lin 2004) mostly due to their cleaning functions as well as to their bright
colors, characteristics that places them between the preferred ornamental species of marine invertebrates (e.g.
Calado et al. 2003a). In the particular case of Thor amboinensis (De Man, 1888) commonly known as the sexy
shrimp in reference to its usually raised tail and to the curious body movements when walking swaying its
abdomen back and forward with exotic elegance, this fascinating behavior as well as their beautiful colors
contribute to its popularity on the ornamental industry (Debelius 2001; Calado et al. 2006). T. amboinensis is a
small hippolityd shrimp with a circum-tropical distribution (Debelius 2001), usually living free or occurring
associated with corals and anemones like Telmatactis cricoides, Heteractis sp., Condylactis gigantea and
Bartholomea annulata (Guo et al. 1996; Wirtz 1997; Debelius 2001; Araújo & Calado 2003). T. amboinensis is a
protandric hermaphrodite that first matures as male, changing to female later in life (Baeza & Piantoni 2010).
The very recent phylogenetic analysis of the combined dataset of two nuclear protein-coding genes (enolase
and sodium-potassium ATPase α-subunit) and one mitochondrial gene (16S rRNA) rejected the monophyletic
status of the family Hippolytidae sensu De Grave & Fransen (2011), therefore the authors considered the
resurrection of the families Lysmatidae Dana, 1852, Thoridae Kingsley, 1879, Bythocarididae Christoffersen 1987
and Merguiidae Christoffersen 1990 (De Grave et al. 2014). According to the authors, family Thoridae Kingsley,
1879 includes the genera Birulia, Eualus, Heptacarpus, Lebbeus, Paralebbeus, Spirontocaris, Thinora and Thor,
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but still needs a full morphological analysis in order to find more defining characters for it. A just published paper
aimed to verify if an improved taxonomic sampling is a necessary and sufficient condition for resolving inter-
families relationships in Caridean decapods (Aznar-Cormano et al. 2015). The authors, using at least two species of
two different genera for each family or subfamily together with all the potential molecular markers, confirmed that
Hippolytidae as defined in De Grave & Fransen (2011) is not monophyletic, and the close relationships of Eualus
gaimardii and Lebbeus polaris strongly support the monophyly of the resurrected family Thoridae by De Grave et
al. (2014).
The genus Thor Kingsley, 1878a is represented by 12 species (De Grave & Fransen 2011), of which only 3
(25%) have their complete larval descriptions known (e.g. Terossi et al. 2010): an undetermined species of Thor
from Bermuda with six zoeal stages and one decapodid described by Lebour (1940), T. floridanus with eight zoeal
stages and one decapodid by Broad (1957), and T. dobkini with two zoeal stages and one decapodid by Dobkin
(1968). In 1938–1939, Lebour found in Bermuda Biological Station a very small conspicuously colored hippolytid
larva common in the plankton. The author collected the first zoeal stage at night and kept it in the laboratory
describing its six zoeal stages and one decapodid (Lebour 1940). After the moult of the decapodid to the first
juvenile, she noticed the resemblance of the rostrum’s shape of the stage obtained with that of the young form
figured by Verrill (1922), concluding that the larval stages obtained by her belonged to Thor (Lebour 1940). Only
in 1957, Broad presented a complete larval description for the genus from laboratory-reared material of T.
floridanus, which has eight zoeal stages and one decapodid (Broad 1957). The author discussed Lebour’s results
concluding that the larvae described by him were quite similar to those previously obtained by her. The third
species for which the complete larval description is known is T. dobkini, with only two zoeal stages and one
decapodid (Dobkin 1968), first named as T. floridanus Kingsley, 1878a. In 1972, Chace assigned T. floridanus
Kingsley, 1878a to a new species, that he called Thor dobkini (Chace 1972).
Considering T. amboinensis, Yang & Okuno (2004) described the first larval stage of the species hatched in the
laboratory, from an ovigerous female collected in Japan (Izu Peninsula). The authors, based on their own larval
description and that of T. floridanus by Broad (1957), defined the larval characters for a first zoea of Thor: rostrum
absent; carapace with anterior and posterior dorsomedian papillae, without midventral or posteroventral denticles;
the antennal scale terminally segmented; the endopod of the maxillule two-segmented, and the distal segment with
three terminal setae; the proximal coxal endite of the maxilla present; the basis of the second maxilliped with nine
setae arranged as 1, 2, 3 and 3; and the exopods of the maxillipeds bearing three terminal asymmetrically disposed
natatory setae. The authors concluded that detailed descriptions of other larvae of Thor were needed for further
characterization of the larval development of the genus. The few existing larval descriptions and the lack of
knowledge on the larval morphology and development of the species of Thor are two of the bottlenecks that are
impairing the captivity production of this shrimp species, since the rearing potential of the species is still unknown
and the sustainability as well as the ecological impacts of harvesting it from nature are poorly studied. More than
ten years ago, Calado et al. (2003a) classified T. amboinensis as a species with the commercial culture techniques
being developed, although until now, the larval development is still unknown. One of the purposes of present work,
therefore, is to describe the complete larval development of T. amboinensis, hatched in the laboratory, comparing
the morphological larval characteristics of this species with those presented by previous authors, revising and
discussing the general morphological features of the larvae of Thor.
Presently, an integrative taxonomical approach for the study of biodiversity has been developed, where the
morphological characters are assigned to the molecular analysis (e.g. Meyer et al. 2013; Marco-Herrero et al.
2015). Knowing that the DNA barcode corresponding to the 650 bp fragment of the folmer region of the
mitochondrial gene cytochrome c oxidase I (COI) has been pointed as the core of a global bio identification system
at the species-level (Hebert et al. 2003), the DNA barcodes of the spent females were obtained. Since different
molecular markers show different evolutionary scenarios for the same taxa (e.g. Bracken et al. 2009, Aznar-
Cormano et al. 2015), and having the molecular identification of the spent females through DNA barcode, we also
aim to verify the recently published hypothesis of the resurrection of the family Thoridae, giving the barcode
perspective (species level) of the phylogenetic reconstruction of the relationships within the family as defined by
De Grave et al. (2014).
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COMPLETE LARVAL DEVELOPMENT OF THOR AMBOINENSIS
Material and methods
Specimen collection and larval culture. Thor amboinensis specimens were collected from their natural habitat,
Philippines (western Pacific), imported to Portugal for commercial purposes, and kept in the laboratory of
LusoReef, in groups of 18 individuals, 9 females and 9 males. The brood stock was maintained in 40 L tanks,
separated from the hatching area by a net, at a salinity of 35 ± 1, temperature of 26.5 ± 1 ºC and a photoperiod of 12
h light: 12 h dark. Five females were preserved in ethanol 70% for further molecular analysis.
The newly hatched larvae attracted by fluorescent light above the brood stock tanks, were collected by a siphon
and stocked at a density of about 40 larvae L
-1
in 10 L cylindrico-conical
recirculation tanks (Calado et al. 2003b).
The salinity was kept at 35 ± 1 and the temperature was maintained at 26.5 ± 1 ºC. The larvae were fed daily with
newly hatched Artemia sp. at a density of 10,000 nauplii.L
-1
. Ten randomly selected larvae were sampled daily and
preserved in 4% formalin for later observation.
Larval drawings and measurements. Drawings and measurements were made with a camera lucida on a
binocular Stereomicroscope Olympus SZX12 and on a Microscope Olympus BX51. The preparation of slides was
temporary. The larval descriptions followed the method proposed by Clark et al. (1998). The setal terminology is in
accordance with Garm (2004). The long aesthetascs on antennules as well as the long plumose setae on the distal
end of the exopods and on the pleopods and uropods were drawn truncated; the setules from setae were omitted
from drawings when necessary. The number of examined specimens per stage is referred in the description (N).
The measurements taken were: total length (TL), corresponding to the distance from the tip of the rostrum to the
posterior end of telson; carapace length (CL), measured from the tip of rostrum to the posterior margin of carapace;
and rostrum length (RL), corresponding to the distance from the tip of rostrum to the eye socket (except in the first
zoea where it was measured from the tip of rostrum to an imaginary line crossing the orbital margin). Ten
specimens of each larval stage were measured. The larval series has been deposited in IPMA—Instituto Português
do Mar e da Atmosfera, in Lisbon, Portugal (IPIMAR/H/Ta/01/2011).
DNA extraction, amplification and sequencing. The species identification was accompanied by the barcode
region of the mitochondrial cytochrome oxidase I gene of the spent females. Five of the nine females were selected,
and for each female a small piece of tissue (muscle removed from the pleon) was used to extract DNA with the
E.Z.N.A. Mollusc DNA Kit (Omega Bio-tek), following the manufacturer protocol. An approximately 650 base
pairs of the COI-5P was amplified from diluted genomic DNA by polymerase chain reaction (PCR), thermal
cycles: 1) denaturation at 94°C for 1 min; 2) denaturation at 94°C (30 s), annealing at 45°C (1 min 30 s), extension
at 72°C for 1 min (5 cycles); 3) denaturation at 94°C (30 s), annealing at 51°C (1 min 30 s), extension at 72°C for 1
min (45 cycles) and a final extension of 5 min at 72°C), using the enhanced primers LoboF1 (KBT CHA CAA
AYC AYA ARG AYA THG G) and Lobo R1 (TGR TTY TTY GGW CAY CCW GAR GTT TA) (Lobo et al.
2013). The PCR products were sequenced bidirectionally using the BigDye Terminator 3 kit, and were run on an
ABI 3730XL DNA analyzer (all from Applied Biosystems™).
Sequence analysis. Sequences were confirmed by sequencing both strands, that were cleaned and edited using
Bio- Edit (http://www.mbio.ncsu.edu/bioedit/bioedit.html) to generate a consensus sequence for each specimen
(four sequences with 658 bp and one with 632 bp). The final sequences were blasted (Basic Local Alignment
Search Tool, BLAST, National Center for Biotechnology Information, NCBI) on GenBank database (http://
www.ncbi.nlm.nih.gov/genbank/) to get the best BLAST matches for an accurate identification. The females used
for the molecular identification of T. amboinensis were deposited in MUHNAC—Museu Nacional de História
Natural e da Ciência, in Lisbon, Portugal, and are catalogued in GenBank under accession numbers (KU201280 to
KU201284).
COI phylogenetic analysis. To provide a phylogenetic context, the sequences obtained by present study for T.
amboinensis were aligned with those available in GenBank for the recently resurrected family Thoridae (De Grave
et al. 2014). In De Grave’s et al. (2014) hippolytoid systematics revision tree the strong nodal support clade,
corresponding to the family Thoridae, had as sister clade the Hippolytidae sensu lato with a weak support, where
the genus Saron among others was clustered. For this reason, Saron marmoratus was considered as the outgroup.
The taxa, vouchers information, sampling localities, accession numbers, and references are summarized in Table 1.
Sequences were manually aligned, carefully checked for the detection of ambiguities and translated to amino acids
for the inspection of stop codons. The uncorrected pairwise distances were calculated to compare the divergences
amongst the selected taxa. The alignment was then verified, using the Muscle tool (Edgar 2004a, 2004b)
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incorporated into MEGA version 6.0 software (Tamura et al. 2013), selecting the “align codons” tool. After the
obtention of the final alignment, the best fitting model of DNA evolution was found for the estimation of the
phylogenetic reconstruction. The resultant model (Tamura 3-parameter) was used to construct the maximum
likelihood (ML) tree following the protocol described in Hall (2013), assessing the confidence in the resulting tree
topology with the non-parametric bootstrap estimates (Felsenstein 1985) with 10000 iterations. All the analysis
were implemented in MEGA version 6.0 (Tamura et al. 2013).
Results
DNA barcode identification and phylogenetic relationships within the family Thoridae. The traditional
morphological description of the larvae of T. amboinensis coupled with the molecular identification of the five
spent females gives significance to the taxonomy of decapod larvae, so the COI sequences obtained for the selected
specimens (GenBank accession Nos KU201280 to KU201284, respectively) were blasted into GenBank for species
matching (BLAST utility, http://blast.ncbi.nlm.nih.gov/Blast.cgi). The closest match (94% similarity) of the
obtained sequences with 632 to 658 bp is T. ambo i nensi s from the north shore of Moorea in the French Polynesia
(GenBank accession No JQ180245.1, with 614 bp). There is another sequence for the same region of COI for T.
amboinensis available in GenBank (accession No GQ260961, with 658 bp ), collected in Palmyra Atoll in the Line
Islands, corresponding to a 98–99% query but only to 87–89% identity. The fast evolving COI gene differentiated
small divergences within the population of the Philippines (0.0–1.2 %). Among the identified populations of T.
amboinensis the uncorrected pairwise distances (p-distance) was higher, varying from 6.8–7.2 % between the
Philippines and Moorea, to 14.3–15.8 % between those and Palmyra Atoll.
We also aimed to explore the utility of the barcode data to verify the recently published hypotheses of the
resurrection of the family Thoridae (Fig. 1). The monophyly of the genera Lebbeus, Spirontocaris and Thor is
strongly supported. The genus Eualus was splitted in three different clades, one of which corresponds to Eualus
cranchii, curiously grouped together with Thor amboinensis. The paraphyly of the genus Eualus, and a probable
reassignment for E. cranchii are suggested. De Grave et al. (2014) assigned E. cranchii to the genus Thoralus to
facilitate the discussion and the comparison with previous classification, without the intent of the resurrection of
the genus.
Complete larval description of Thor amboinensis. Eight zoeal stages and one decapodid were identified.
Under laboratory conditions the molt to decapodid occurred 28 days after hatching. The first zoeal and the
decapodid stages are described in detail, whereas for the second to the eighth zoeae only the morphological
differences from the previous stages are mentioned.
Thor amboinensis (De Man, 1888)
(Figures 2–6)
First zoea
Dimension: TL= 1.99–2.30 mm; CL= 0.53–0.65 mm; N= 5.
Carapace (Figs. 2A): rostrum absent; eyes sessile; anterior and posterior dorsomedian papillae present;
pterygostomian spine present.
Antennule (Fig. 2B): peduncle unsegmented, with 1 long plumose seta terminally; short outer flagellum with 4
aesthetascs and 1 plumose seta terminally.
Antenna (Fig. 2C): protopod unsegmented, with 1 small distal spine; endopod with 1 small serrulate and 1 long
terminal plumose setae (the small seta with approximately one fifth of the length of the long plumose seta);
scaphocerite 5-segmented, 4 short segments distally, with 9 plumose setae on inner margin, 2 plumose setae on
outer margin, and 1 small simple seta on apex.
Mandibles (Fig. 2D): asymmetrical, palps absent; armature of incisor and molar processes as illustrated; left
mandible with 1 fan-like lacinia mobilis.
Maxillule (Fig. 2E): coxal endite with 6 papposerrate setae, basial endite with 5 cuspidate setae; endopod 2-
segmented: proximal segment with 1 short simple and 2 strong papposerrate setae, distal segment with 3 strong
terminal papposerrate setae. Microtricha as illustrated.
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COMPLETE LARVAL DEVELOPMENT OF THOR AMBOINENSIS
TABLE 1 Specimens of the family Thoridae and of the outgroup used for the molecular phylogenetic reconstruction, with the respective site of collection, Genbank accession number (COI),
and published reference.
Taxon Sampling locality GenBank Accession Nr (COI) Reference
Eualus avinus (Rathbun, 1899) Northeast Pacific (Canada) DQ882065 Costa et al. (2007)
Eualus barbatus (Rathbun, 1899) Northeast Pacific (Canada) DQ882070 Costa et al. (2007)
Eualus biunguis (Rathbun, 1902a) Northeast Pacific (Canada) DQ882074 Costa et al. (2007)
Eualus cranchii (Leach, 1817) Northeast Atlantic (Portugal) KF369190 Lobo et al. (2013)
Eualus fabricii (Krøyer, 1841) Northwest Atlantic (Canada) FJ581628 Radulovici et al. (2009)
Eualus gaimardii (H. Milne Edwards, 1837) Northwest Atlantic (Canada) FJ581629 Radulovici et al. (2009)
Eualus macilentus (Krøyer, 1841) Northwest Atlantic (Canada) FJ581635 Radulovici et al. (2009)
Lebbeus antarcticus (Hale, 1941) South Atlantic (Scotia Sea) KC494752 Nye et al. (2013)
Lebbeus carinatus Zarenkov, 1976 Northeast Pacific (Vents 13ºN) AF125422 Shank et al. (1999)
Lebbeus groenlandicus (Fabricius, 1775) Northwest Atlantic (Canada) FJ581737 Radulovici et al. (2009)
Lebbeus polaris (Sabine, 1824) North Atlantic (Norway) KP759420 Aznar-Cormano et al. (2015)
Eualus suckleyi (Stimpson, 1864) Northeast Pacific (Canada) DQ882078 Costa et al. (2007)
Lebbeus virentova (Nye et al., 2012) West Atlantic (Mid-Cayman Spreading Center) KJ566966 Plouviez et al. (2015)
Spirontocaris holmesi Holthuis, 1947a Northeast Pacific (Canada) DQ882153 Costa et al. (2007)
Spirontocaris lamellicornis (Dana, 1852a) Northeast Pacific (Canada) DQ882157 Costa et al. (2007)
Spirontocaris lilljeborgii (Danielssen, 1859) Northwest Atlantic (Canada) FJ581903 Radulovici et al. (2009)
Spirontocaris phippsii (Krøyer, 1841) Arctic Ocean (Canada) DQ882159 Costa et al. (2007)
Spirontocaris sica Rathbun, 1902a Northeast Pacific (Canada) DQ882161 Costa et al. (2007)
Spirontocaris spinus (Sowerby, 1805) Arctic Ocean (Canada) DQ882163 Costa et al. (2007)
Thor amboinensis (De Man, 1888b) Pacific Ocean (Palmyra Atoll) GQ260961 Plaisance et al. (2009)
Pacific Ocean (Moorea) JQ180245 Unpublished
Pacific Ocean (Philippines) KU201280 Present study
Pacific Ocean (Philippines) KU201281 Present study
Pacific Ocean (Philippines) KU201282 Present study
Pacific Ocean (Philippines) KU201283 Present study
Pacific Ocean (Philippines) KU201284 Present study
Saron marmoratus (Olivier, 1811)* South Pacific Ocean (New Caledonia) KP759508 Aznar-Cormano et al. (2015)
*Outgroup.
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FIGURE 1. Phylogenetic tree of representatives of the family Thoridae and one outgroup based on the mitochondrial
cytochrome c oxidase I (COI) barcode gene sequences (658 bp). Sequences were aligned with those available in GenBank. The
phylogenetic reconstruction was carried out with the Maximum Likelihood (ML) analysis, implemented in MEGA version 6.0
(Tamura et al. 2013). Numbers are support values for 10000 bootstraps.
Maxilla (Fig. 2F): coxal endite bilobed with 8 + 4 papposerrate setae; basial endite bilobed with 4+ 4
papposerrate setae; endopod unsegmented, trilobed, bearing 3+2+1+3 papposerrate setae; scaphognathite with 5
marginal plumose setae, and microtricha on inner margin.
First maxilliped (Fig. 2G): coxa with 4–5 papposerrate setae; basis with 13 papposerrate setae; endopod 4-
segmented, with 3, 1, 2, 1+3 papposerrate setae; exopod unsegmented, with 1 shorter seta subapically on lateral
margin and 3 long terminal plumose setae.
Second maxilliped (Fig. 2H): coxa with 1 papposerrate seta; basis with 9 papposerrate setae arranged as 1, 2, 3,
3; endopod 4-segmented with 3, 1, 2 and 1+4 papposerrate terminal setae; exopod unsegmented, with 2
subterminal and 3 terminal plumose setae.
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Third maxilliped (Fig. 2I): coxa unarmed; basis with 3 papposerrate setae; endopod 4-segmented with 2, 1, 2
and 1+3 papposerrate setae; exopod unsegmented, with 2 subterminal and 3 terminal plumose setae.
First pereiopod (Fig. 2J): present as a small biramous bud.
Second to fifth pereiopods: absent.
Pleon (Fig. 2A): 5 smooth pleomeres; third pleomere distinctly curved; fourth pleomere with a pair of dorsal
simple setae and a small tuft of 5–6 simple setae.
Pleopods: absent.
Uropods: absent.
Telson (Fig. 2K): triangular, indented medially, with 7+7 setae (inner 5 plumose and the outer 2 plumose only
on proximal axis); minute spines between and around the setae, as illustrated.
Second zoea
Dimension: TL= 2.16–2.50 mm; CL= 0.65–0.79 mm; N= 6.
Carapace (Figs. 2L): eyes stalked, with ocular peduncle shorter than antennal peduncle; rostrum present,
triangular, not extending beyond the eyes.
Antennule (Fig. 2M): peduncle 2-segmented, with 1 small plumose seta on the inner margin positioned at
about one third the length of the first segment, and distal segment with 2 short and 1 long plumose setae terminally;
outer flagellum with 5 aesthetascs and 1 spinous process terminally.
Antenna (Fig. 2N): scaphocerite 4-segmented, 3 short segments distally, with 9 plumose setae on inner margin,
2 plumose setae on outer margin, and 1 small simple seta on apex.
Mandibles: unchanged.
Maxillule: coxal endite with 6–7 papposerrate setae, basial endite with 6 cuspidate setae.
Maxilla: coxal endite bilobed with 8–9 + 4 papposerrate setae; basial endite bilobed with 4–5+ 4–5
papposerrate setae.
First maxilliped: coxa with 6–7 papposerrate setae; basis with 13–14 papposerrate setae; exopod with 1 shorter
seta subapically and 4 long terminal plumose setae.
Second maxilliped: endopod 4-segmented with 3+1, 1, 2 and 1+5 papposerrate terminal setae; exopod
unsegmented, bearing 2 subterminal and 4 terminal plumose setae.
Third maxilliped: coxa unarmed; basis with 3 papposerrate setae; endopod 5-segmented with 2, 1, 0, 2, 1+3
papposerrate setae; exopod unsegmented, with 2 subterminal and 4 terminal plumose setae.
First pereiopod (Fig. 2O): biramous bud enlarged in size.
Second pereiopod (Fig. 2P): present as a small biramous bud.
Third to fifth pereiopods: absent.
Pleon (Fig. 2L): unchanged.
Pleopods: absent.
Uropods: absent.
Telson (Fig. 2Q): 8+8 plumose setae, outer seta plumose on proximal axis only.
Third zoea
Dimension: TL= 2.52–2.74 mm; CL= 0.74–0.84 mm; N= 5.
Carapace (Fig. 3A): pterygostomian spine followed by 1 very small denticle in the ventral margin. Otherwise
unchanged besides size.
Antennule: peduncle 2-segmented, proximal segment with 2–3 small plumose setae positioned at two thirds of
the length of the segment, and 3–4 small plumose setae distally; distal segment with 2 long+ 4–6 short plumose
setae terminally; small inner flagellum with 1 long plumose seta; outer flagellum with 2 aesthetascs, 1 small
spinous process, 1 plumose and 1 sparsely plumose setae terminally.
Antenna: scaphocerite 3-segmented, 2 short segments distally, with 11 plumose setae on inner margin, 2
plumose setae on outer margin, and 1 small simple seta on apex.
Mandibles: right mandible with 1 fan-like lacinia mobilis, otherwise unchanged.
Maxillule: basial endite with 7–8 cuspidate setae.
Maxilla: proximal coxal endite with 10–12 papposerrate setae; scaphognathite with 7 marginal plumose setae.
Maxilla: unchanged.
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First maxilliped: basis with 14–15 papposerrate setae; exopod unsegmented, with 1 shorter seta at one third of
the length of the segment, 1 shorter seta subapically on lateral margin and 4 long terminal plumose setae.
Second maxilliped (Fig. 3B): endopod 5-segmented with 3+1, 1, 0, 2 and 1+5 papposerrate terminal setae,
microtricha present on first segment inner margin.
Third maxilliped: unchanged.
First pereiopod (Fig. 3C): functional; biramous; basis unarmed; endopod 5-segmented, with 0, 0, 0, 2, 1+2
papposerrate setae; exopod unsegmented, with 2 subterminal and 4 terminal plumose setae.
Second pereiopod (Fig. 3D): unchanged, besides size.
Third pereiopod (Fig. 3E): present as a small biramous bud.
Fourth and fifth pereiopods: absent.
Pleon: 6 pleomeres; without spines; the third pleomere distinctly curved; the fourth pleomere with a pair of
dorsal simple setae and a small tuft of 5 simple setae.
Pleopods: absent.
Uropods (Fig. 3F): biramous; endopod small with 2 short plumose setae apically; exopod well developed
almost reaching the end of telson, with 6 marginal plumose setae; microtricha as illustrated.
Telson (Fig. 3F): separated from sixth pleomere, with a pair of lateral short simple setae followed by 7+7
plumose setae.
Fourth zoea
Dimension: TL= 2.98–3.38 mm; CL= 0.84–0.94 mm; N= 5.
Carapace: unchanged.
Antennule: peduncle 2-segmented, proximal segment with 5–6 plumose setae distributed along inner margin,
1+1 small plumose setae on stylocerite, 1 strong spine at half the length of the segment, 3–4 small plumose setae
positioned at three-quarters the length of the segment, and 4 small plumose setae distally; distal segment with 4
long+ 4 short plumose setae and 1 simple seta terminally; small inner flagellum with 1 long plumose seta; outer
flagellum with 2 aesthetascs, 1 plumose and 1 sparsely plumose setae terminally.
Antenna (Fig. 3G): endopod small and pointed; scaphocerite unsegmented and rounded terminally, with 14–16
plumose setae along inner and posterior margin, 1 small simple seta on outer margin at half the length of the
antennal scale.
Mandibles: right mandible with 1 submarginal process between lacinia mobilis and molar process.
Maxillule (Fig. 3H): coxal endite with 7–8 papposerrate setae, basial endite with 8–9 cuspidate setae.
Maxilla (Fig. 3I): coxal endite with 10–12+ 4–5 papposerrate setae; basial endite with 5–6+ 5–6 papposerrate
setae; scaphognathite with 10 marginal plumose setae.
First maxilliped: coxa with 7 papposerrate setae; basis with 13–15 papposerrate setae; endopod and exopod
unchanged.
Second maxilliped: unchanged.
Third maxilliped: coxa unarmed; basis with 3 papposerrate setae; endopod 5-segmented, with 2, 1, 1, 2 and
1+4 papposerrate setae; exopod unsegmented, with 2 subterminal and 4 terminal plumose setae.
First pereiopod: basis with 1+1 papposerrate setae; endopod 5-segmented, with 1, 0, 0, 2, 1+3 papposerrate
setae; exopod unsegmented, with 2+ 2+ 4 plumose setae.
Second pereiopod (Fig. 3J): functional; biramous; basis unarmed; endopod feebly segmented, with 1 subterminal
and 2 terminal papposerrate setae; exopod unsegmented, with 1 subterminal and 3 terminal plumose setae.
Third pereiopod (Fig. 3K): unchanged besides size.
Fourth and fifth pereiopods: absent.
Pleon: unchanged.
Pleopods: absent.
Uropods (Fig. 3L): protopod unarmed; endopod with 7–8 plumose setae, distributed along distal and inner
margins; exopod as long as telson, with 1 spine on apex followed by 9–11 marginal plumose setae, and 1 plumose
seta on dorsal distal margin; microtricha as illustrated.
Telson (Fig. 3L): rectangular, with 1 pair of lateral spines and 7 pairs of terminal posterior processes (2 pairs of
outer spines followed by 5 pairs of plumose setae on the posterior end, being the outermost pair the longest and the
2 inner pairs the shortest).
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Fifth zoea
Dimension: TL= 3.35–3.85 mm; CL= 0.89–1.00 mm; N= 6.
Carapace (Fig. 3M): unchanged.
Antennule (Fig. 3N): peduncle 2-segmented, proximal segment with 6–7 plumose setae, distributed along
inner margin, 2–3 small plumose setae on stylocerite, 1 strong spine at half the length of the segment, 5–6 small
plumose setae positioned at three-quarters the length of the segment, and 4–6 small plumose setae distally; distal
segment with 4–5 long+ 5 short plumose setae and 2 simple setae terminally; small inner flagellum with 1 long
plumose seta; outer flagellum with 3 aesthetascs and 2 plumose setae terminally.
Antenna: protopod with 1+ 1 spines; endopod pointed at its posterior end, with approximately one third of the
length of the antennal scale; scaphocerite unsegmented, with 15–16 plumose setae along inner and posterior margin
and 1 small simple seta on outer margin at half the length of the antennal scale.
Mandibles: left mandible with 1 submarginal process between lacinia mobilis and molar process. Otherwise
unchanged.
Maxillule: coxal endite with 9–10 papposerrate setae, basial endite with 10–11 cuspidate setae.
Maxilla: proximal coxal endite with 11–12 papposerrate setae; basial endite bilobed with 5–6+ 5–6
papposerrate setae; endopod unchanged; scaphognathite with 14–16 marginal plumose setae.
First maxilliped: coxa with 7–8 papposerrate setae; basis with 17–19 papposerrate setae; endopod 4-segmented
with 4, 1, 2, 1+3 papposerrate setae; epipod bud present.
Second maxilliped: endopod 5-segmented with 3+1, 1, 1, 2 and 1+5 papposerrate terminal setae.
Third maxilliped: basis with 2 papposerrate setae; exopod unsegmented, with 0–1+ 2+ 4 plumose setae.
First pereiopod: basis with 2 papposerrate setae; endopod 5-segmented, with 1, 1, 1, 2, 1+3 papposerrate setae;
exopod unsegmented, with 0–1+ 2+ 2+ 4 plumose setae.
Second pereiopod: basis with 2 papposerrate setae; endopod 5-segmented, first four segments with 1, 0, 0, 2
papposerrate setae, terminal segment with1 subterminal+ 2 terminal papposerrate setae and 1 minute projection at
its distal end; exopod unsegmented, with 2+ 2+ 4 plumose setae.
Third pereiopod (Fig. 3O): functional; basis unarmed; endopod unsegmented, with 2 small simple setae
terminally; exopod unsegmented, with 2+ 4 plumose setae.
Fourth pereiopod (Fig. 3P): present as a very small uniramous bud.
Fifth pereiopod (Fig. 3P): present as a very small uniramous bud.
Pleon: unchanged.
Pleopods: absent.
Uropods (Fig. 3Q): protopod unarmed; endopod with 5–6 short plumose setae proximally on outer margin, 10–
12 plumose setae along distal and inner margins, 3 plumose setae on dorsal distal margin; exopod longer than
telson, with 1 short plumose seta proximally on outer margin, 1 simple seta on apex followed by 14–15 marginal
plumose setae, and 2–3 plumose setae on dorsal distal margin.
Telson (Fig. 3Q, Q’): margins laterally parallel, slightly narrower posteriorly, with 2 pairs of lateral spines, 1
pair of small outer spines, followed by 1 pair of plumose setae on inner margin (the longest), 1 pair of simple setae
and 3 pairs of plumose setae on the posterior end.
Sixth zoea
Dimension: TL= 3.62–3.85 mm; CL= 0.92–1.04 mm; N= 6.
Carapace (Fig. 4A): unchanged besides size.
Antennule: peduncle 2-segmented, proximal segment 7–8 plumose setae distributed along inner margin, 2–3
small plumose setae on stylocerite, 1 strong spine at half the length of the segment, 6–7 small plumose setae
positioned at three-quarters the length of the segment, and 5–6 small plumose setae distally; distal segment with 5
long+ 4–5 short plumose setae and 2 simple setae terminally; small inner flagellum with 1 long plumose seta; outer
flagellum with 2 subterminal+3 terminal aesthetascs and 2 plumose setae distally.
Antenna (Fig. 4B): endopod unsegmented, reaching half length of the antennal scale, with 1 short simple seta
terminally; scaphocerite with 17–18 plumose setae along inner and posterior margin.
Mandibles: unchanged.
Maxillule: basial endite with 11–12 cuspidate setae.
Maxilla: proximal coxal endite with 11–12+ 4–6 papposerrate setae; bilobed basial endite each with 6–7+ 6–7
papposerrate setae; scaphognathite with 15–16 marginal plumose setae.
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First maxilliped: basis with 17–18 papposerrate setae; epipod enlarged in size.
Second maxilliped: coxa with 1–2 papposerrate setae.
Third maxilliped: unchanged besides size.
First pereiopod: basis with 2 papposerrate setae; endopod 5-segmented, with 2, 1, 1, 2, 1+4 papposerrate setae;
exopod unsegmented, with 1+ 2+ 2+ 4 plumose setae.
Second pereiopod: basis with 2 papposerrate setae; endopod 5-segmented, with 1, 1, 1, 2, 1+ 3 papposerrate
setae; exopod unsegmented, with 1+ 2+ 2+ 4 plumose setae.
Third pereiopod (Fig. 4C): basis unarmed; endopod 5-segmented, first four segments with 1, 0, 0, 1
papposerrate setae, terminal segment with 1 subterminal+ 2 terminal papposerrate setae and 1 minute spine at its
distal end; exopod unsegmented, with 1+ 2+ 2+ 4 plumose setae.
Fourth pereiopod (Fig. 4D): unchanged besides size.
Fifth pereiopod (Fig. 4E): unchanged besides size.
Pleon (Fig. 4A): fifth pleomere pleura rounded.
Pleopods (Fig. 4A): present as very small buds.
Uropods (Fig. 4F): protopod unarmed; endopod with 6–7 short plumose setae proximally on outer margin, 14–
15 plumose setae along distal and inner margins, 4 plumose setae on dorsal distal margin; exopod with 1 short
plumose seta proximally+ 2 simple setae distally on outer margin, 1 simple seta on apex followed by 17–19
marginal plumose setae, and 4–5 plumose setae on dorsal distal margin.
Telson (Fig. 4F): tapering towards the posterior end, bears 2 pairs of lateral spines, followed by 1 pair of small
outer spines and 4 pairs of setae on the posterior end (first longest pair plumose on the inner margin, second pair
simple and the two inner pairs plumose).
Seventh zoea
Dimension: TL= 4.08–4.38 mm; CL= 1.04–1.19 mm; N= 7.
Carapace (Fig. 4G): unchanged.
Antennule (Fig. 4H): peduncle 3-segmented, first segment with 5 plumose setae distributed along inner
margin, 3 small plumose setae on stylocerite, 1 strong spine at half the length of the segment, and 6–7 small
plumose setae terminally; second segment with 2 plumose setae distributed along inner margin and 5–7 small
plumose setae distally; third and distal segment with 5 long+ 4–5 short plumose setae and 2 simple setae
terminally; inner flagellum unsegmented, with 1 long plumose seta; outer flagellum 2-segmented, proximal
segment with 2 terminal aesthetascs, distal segment with 1 subterminal+3 terminal aesthetascs and 2 plumose setae
terminally.
Antenna: endopod 4-segmented, with approximately three quarters of the length of the antennal scale, with 3
short simple setae terminally in distal segment; scaphocerite with 1 short plumose seta followed by 18 plumose
setae along inner and posterior margin.
Mandibles: left and right mandibles each with 2 submarginal processes between the laciniae mobiles and the
molar processes.
Maxillule (Fig. 4I): basial endite with 12–13 cuspidate setae.
Maxilla (Fig. 4J): coxal endite with 11–12+ 4–6 papposerrate setae; basial endite bilobed with 6–7+ 6–7
papposerrate setae; endopod with 4+2+1+3 papposerrate setae; scaphognathite with 17–18 marginal plumose setae.
First maxilliped (Fig. 4K): coxa with 6–7 papposerrate setae; basis with 16–18 papposerrate setae; exopod
bearing 1 shorter seta at one third of the length of the segment, 1 shorter seta subapically on lateral margin and 4
long terminal plumose setae; epipod enlarged in size.
Second maxilliped (Fig. 4L): unchanged besides size.
Third maxilliped (Fig. 4M): coxa unarmed; basis with 1–2 papposerrate setae; endopod 5-segmented, with 2,
1, 1, 2, 1+4 papposerrate setae; exopod unsegmented, with 2+ 2+ 4 plumose setae.
First pereiopod: basis with 1–2 papposerrate setae; endopod subchelate, with internal distal margin of
propodus produced forward to about one-third of dactylus, 5-segmented, with 2, 2, 2, 2, 1+4 papposerrate setae;
exopod with 2+ 2+ 2+ 4 plumose setae.
Second pereiopod: basis with 1–2 papposerrate setae; endopod subchelate, with internal distal margin of
propodus produced forward to about one-third of dactylus, 5-segmented, with 1, 1–2, 1, 2, 1+3 papposerrate setae;
exopod with 2+ 2+ 2+ 4 plumose setae.
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Third pereiopod (Fig. 4N): basis unarmed; endopod 5-segmented, first four segments with 1, 0, 0, 2
papposerrate setae, terminal segment with1 subterminal+ 2 terminal papposerrate setae and 1 minute projection at
its distal end; exopod unsegmented, with 1+ 2+ 2+ 4 plumose setae.
Fourth pereiopod (Fig. 4O): functional; basis with 1 papposerrate setae; 5-segmented, ischium, merus and
carpus naked; propodus with 1 small papposerrate seta terminally; dactylus with 1 papposerrate seta at one third the
length of the segment+ 1 subterminal papposerrate seta and 1 minute projection at its distal end.
Fifth pereiopod (Fig. 4P): functional; basis unarmed; 5-segmented, ischium, merus and carpus unarmed;
propodus with 1 small papposerrate seta terminally; dactylus with 1 papposerrate seta subterminally and 1 minute
projection at its distal end.
Pleon (Fig. 4G): fourth pleomere with a small tuft of simple small setae.
Pleopods (Fig. 4G, Q): biramous buds.
Uropods: protopod unarmed; endopod with 7–8 short sparsely plumose setae proximally on outer margin, 15–
16 plumose setae along distal and inner margins, and 6–8 plumose setae on dorsal margin; exopod with 1 short
plumose seta proximally+ 2–3 simple setae distally on outer margin, 1 spine on apex followed by 18–19 marginal
plumose setae, and 6–7 plumose setae on dorsal distal margin.
Telson: unchanged besides size.
Eighth zoea
Dimension: TL= 4.31–4.61 mm; CL= 1.15–1.31 mm; N= 5.
Carapace (Fig. 5A): pterygostomian spine followed by 2 small denticles in ventral margin; otherwise
unchanged.
Antennule (Fig. 5B): peduncle 3-segmented, first segment with 5 plumose setae distributed along inner
margin, 3 small plumose setae on stylocerite, 1 strong spine at half the length of the segment, and 9–10 small
plumose setae terminally; second segment with 2 plumose setae, distributed along inner margin and 7–8 small
plumose setae distally; third segment with 5 long+ 5 short plumose setae and 2 simple setae terminally; inner
flagellum unsegmented, with 1 long plumose seta; outer flagellum 3-segmented, first segment with 3 terminal
aesthetascs; second segment with 3 terminal aesthetascs; third segment with 3 subterminal aesthetascs and 2
terminal plumose setae.
Antenna (Fig. 5C): endopod longer than the antennal scale, 8-segmented, with 0–3 simple setae in all
segments, except in the last that bears 3–4 simple setae terminally; scaphocerite with 1 short plumose seta followed
by 20–22 plumose setae along inner and posterior margin.
Mandibles (Fig. 5D): left mandible bearing incisor armature as illustrated, with 1 lacinia mobilis and 4
submarginal processes followed by the molar process; right mandible bearing incisor armature as illustrated, with 1
lacinia mobilis and 2 submarginal processes followed by the molar process.
Maxillule: unchanged.
Maxilla: coxal endite with 11–12+ 5–6 papposerrate setae; scaphognathite with 20–21 marginal plumose setae.
First maxilliped: coxa with 6–8 papposerrate setae; basis with 17–18 papposerrate setae.
Second maxilliped: coxa with 2 papposerrate setae; endopod 5-segmented, with 3+1, 1, 1, 2, 1+6 papposerrate
terminal setae; epipod enlarged in size.
Third maxilliped: coxa unarmed; basis with 1–2 papposerrate setae; endopod 5-segmented with 2, 1, 1, 3 and
1+4 papposerrate setae; exopod unsegmented, with 1+ 2+ 2+ 4 plumose setae; epipod bud present.
First pereiopod (Fig. 5E, E’): basis with 1 papposerrate seta; endopod subchelate, with internal distal margin of
propodus produced forward beyond half the length of dactylus, 5-segmented, with 2, 2, 2, 2, 1+4 papposerrate
setae; exopod unchanged.
Second pereiopod (Fig. 5F): basis with 1 papposerrate seta; endopod subchelate, 5-segmented, with 1, 1, 1, 3,
1+3 papposerrate setae, with internal distal margin of propodus produced forward to about one-third of dactylus;
bearing 1+ 2+ 2+ 2+ 4 plumose setae.
Third pereiopod (Fig. 5G, G’): basis unarmed; endopod 5-segmented, first four segments with 0, 1, 1, 3–4
papposerrate setae; terminal segment with1 subterminal+ 1 terminal papposerrate setae and 2 small spines at its
distal end.
Fourth pereiopod (Fig. 5H): basis with 1 papposerrate seta; 5-segmented, ischium, merus and carpus naked;
propodus with 2 small papposerrate setae terminally; dactylus pointed, with 1 subterminal papposerrate seta.
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Fifth pereiopod (Fig. 5I): basis unarmed; 5-segmented, ischium, merus and carpus naked; propodus with 2
small papposerrate setae terminally; dactylus pointed, with 1 subterminal papposerrate seta.
Pleon (Fig. 5A): unchanged.
Pleopods (Fig. 5A, J–N): protopod naked; first pleopod bearing endopod and exopod with 2+ 2 small spines;
second and third pleopods bearing endopods with 2+ 2 small spines, and exopods also with 2+ 2 small spines
distally; fourth pleopod endopod with a small appendix interna and 2 small spines and exopod with 2 small spines
distally; fifth pleopod bearing endopod with small appendix interna and 2+ 2 small spines and exopod with 2 small
spines distally.
Uropods (Fig. 5O): protopod unarmed; endopod with 10 short sparsely plumose setae proximally on outer and
distal margin, 16–17 plumose setae along distal and inner margins, and 8–10 plumose setae on dorsal margin;
exopod with 1 short plumose seta proximally+ 3–4 simple setae distally on outer margin, 1 spine on apex followed
by 21–22 marginal plumose setae, and 4–5 plumose setae on dorsal distal margin.
Telson (Fig. 5O): rather triangular, narrower distally, with 2 pairs of dorso-lateral spines followed by 1 pair of
lateral spines and 4 pairs of setae as illustrated on the posterior end.
Decapodid
Dimension: TL= 4.41–4.52 mm; CL= 1.08–1.24 mm; N= 2.
Carapace (Fig. 6A): rostrum triangular, broad and short reaching one third of the length of the eye; 1 antennal
spine and 1 pterygostomian spine present; dorsal organ and a small anterior dorsomedian papilla present.
Antennule (Fig. 6B): peduncle 3-segmented, first segment with 6–8 small plumose setae on stylocerite, 1 spine
at half the length of the segment, and 7–8 small plumose+ 1 small simple setae terminally; second segment with 1
plumose seta+ 1 spine+ 5 sparsely plumose+ 1 simple setae distally; third segment with 2 simple+ 4–5 sparsely
plumose setae terminally; inner flagellum 4-segmented, with 0, 2, 2, 4 simple setae; outer flagellum 5-segmented,
first segment with 3 terminal aesthetascs, second segment with 3+ 3 aesthetascs and 1–2 simple setae, third
segment with 3 terminal aesthetascs, fourth segment with 3–4 terminal simple setae, fifth and last segment with 4
terminal simple setae.
Antenna (Fig. 6C): protopod with 1+ 1 spines and 1 simple seta; flagellum composed of 20–21 segments,
being the third segment the longest, with 0–5 simple setae distributed as illustrated; scaphocerite with 1 spine on its
posterior outer margin, followed by 26 plumose setae along inner and posterior margin.
Mandibles (Fig. 6D): armature of incisor and molar processes as illustrated.
Maxillule (Fig. 6E): coxa with 9–10 simple and papposerrate setae; basis with 20–21 cuspidate and
papposerrate setae; endopod slightly bilobed, with 1 sparsely plumose seta on the lower lobe.
Maxilla (Fig. 6F): coxal endite bilobed with 6+ 2 papposerrate setae; basial endite bilobed with 8–9+ 9
papposerrate setae; endopod unsegmented bearing 1+ 1 papposerrate and 1 simple setae distributed as figured;
scaphognathite with 24–25 marginal plumose setae.
First maxilliped (Fig. 6G): coxa with 5–6 papposerrate setae; basis with 24–26 papposerrate setae; endopod
trilobed, with 2+ 1+1 papposerrate setae; exopod with 3 plumose setae on proximal lobe, 1 shorter seta subapically
on lateral margin and 4 long terminal plumose setae; epipod present.
Second maxilliped (Fig. 6H): coxa with 2 papposerrate setae; basis with 8–10 papposerrate setae; endopod 4-
segmented with 1, 1, 6–7, 14–15 papposerrate terminal setae; epipod present.
Third maxilliped (Fig. 6I, I’, I’’): coxa with 1 papposerrate seta; basis with 3 papposerrate setae; endopod 3-
segmented, proximal segment with 2 spines and 4–5 simple setae terminally; median segment with 5–6 simple
setae; distal segment with 19–20 simple setae, distributed as illustrated and 4 strong spines terminally; exopod
measuring approximately half of the exopod, unsegmented, with 3 simple setae terminally.
First pereiopod (Fig. 6J): coxa with 1 simple seta on distal margin; basis with 2 simple setae on lateral margin;
ischium with 1 spine terminally; merus with 2 simple setae terminally; carpus with 5–6 spines as figured and 2
distal simple setae; chela present, propodus with 1 anterior spine, 7–8 simple setae distributed as figured, and stout
distal end, and dactylus with 3 terminal spines and 7–8 simple setae; exopod reduced and unsegmented.
Second pereiopod (Fig. 6K): coxa and basis each with 1 simple seta; endopod more slender than that of the first
pereiopod; ischium and merus each with 2 simple setae, arranged as figured; carpus subdivided in two segments,
with 1–2 simple setae; propodus with stout distal end and 6–7 simple setae, distributed as figured; dactylus forming
chela, bearing stout distal end, with 5–6 simple setae, distributed as figured; exopod reduced and unsegmented,
with 4–5 simple setae terminally.
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FIGURE 2. Thor amboinensis. First zoea: A, total animal, lateral view; B, antennule; C, antenna; D, mandibles; E, maxillule;
F, maxilla; G, first maxilliped; H, second maxilliped; I, third maxilliped; J, first pereiopod; K, telson. Second zoea: L, total
animal, lateral view; M, antennule; N, antenna; O, first pereiopod; P, second pereiopod; Q, telson. Scale bars: 0.5 mm (A, K,
Q); 0.1 mm (B–J, L–P).
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FIGURE 3. Thor amboinensis. Third zoea: A, total animal, lateral view; B, second maxilliped; C, first pereiopod; D, second
pereiopod; E, third pereiopod; F, telson and uropods. Fourth zoea: G, antenna; H, maxillule; I, maxilla; J, second pereiopod; K,
third pereiopod; L, telson and uropods. Fifth zoea: M, total animal, lateral view; N, antennule; O, third pereiopod; P, fourth and
fifth pereiopods; Q, telson and uropods; Q’, detail of telson. Scale bars: 0.5 mm (F, L, O, Q); 0.1 mm (A–E, G–K, M–N, P, Q’).
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COMPLETE LARVAL DEVELOPMENT OF THOR AMBOINENSIS
FIGURE 4. Thor amboinensis. Sixth zoea: A, total animal, dorsal view; B, antenna; C, third pereiopod; D, fourth pereiopod; E,
fifth pereiopod; F, telson and uropods. Seventh zoea: G, total animal, lateral view; H, detail of antennules exopod; I, maxillule;
J, maxilla; K, first maxilliped; L, second maxilliped; M, third maxilliped; N, detail of dactylus of third pereiopod; O, fourth
pereiopod; P, fifth pereiopod; Q, pleopods . Scale bars: 0.5 mm (B, D, E, F); 0.1 mm (A, C, G–M, O–Q).
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FIGURE 5. Thor amboinensis. Eighth zoea: A, total animal, lateral view; B, antennule; C, antenna; D, mandibles; E, first
pereiopod; E’, detail of propodus and dactylus of first pereiopod; F, second pereiopod; G, third pereiopod; G’, detail of
propodus and dactylus of third pereiopod; H, fourth pereiopod; I, fifth pereiopod; J, first pleopod; K, second pleopod; L, third
pleopod; M, fourth pleopod; N, fifth pleopod; O, telson and uropods. Scale bars: 0.5 mm (B, C, E–G, I–O); 0.1 mm (A, D, E’,
G’, H).
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COMPLETE LARVAL DEVELOPMENT OF THOR AMBOINENSIS
FIGURE 6. Thor amboinensis. Decapodid: A, total animal, lateral view; B, antennule; C, antenna; D, mandibles; E, maxillule;
F, maxilla; G, first maxilliped; H, second maxilliped; I, third maxilliped;
I’,
detail of proximal segment of third maxilliped
endopod; I’’, detail of distal segment of third maxilliped endopod; J, first pereiopod; K, second pereiopod; L, third pereiopod;
M, fourth pereiopod; N, fifth pereiopod; O, first pleopod; P, second pleopod; Q, third pleopod; R, fourth pleopod; S, fifth
pleopod; T, telson and uropods; T’, detail of telson. Scale bars: 0.5 mm (B–D, I–T); 0.1 mm (A, E–H, I’, I’’, T’).
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Third pereiopod (Fig. 6L): coxa and basis each with 2 simple setae; ischium, merus and carpus with 1, 4–5, 4–
5 simple setae, arranged as figured; propodus with 2 spines+ 6–7 simple setae distributed as figured and 1 strong
simple+ 1,papposerrate+ 4–5 simple setae terminally; dactylus stout, apically curved, with 3 spines along inner
margin and 2 simple setae terminally; exopod reduced, unsegmented and unarmed.
Fourth pereiopod (Fig. 6M): coxa unarmed; basis with 1 simple seta; ischium, merus and carpus with 3–4, 4–5,
1–2 simple setae, arranged as figured; propodus with 2 spines+ 6–8 simple setae, distributed as figured and 1 strong
simple+ 1papposerrate+ 4–5 simple setae terminally; dactylus stout, apically curved, with 3 spines along inner
margin and 2 simple setae; exopod absent.
Fifth pereiopod (Fig. 6N): coxa unarmed; basis with 2–3 simple setae; ischium, merus and carpus with 3–4, 2–
3, 2–3 simple setae, arranged as figured; propodus with 2 spines+ 6–8 simple setae, distributed as figured and 2
strong simple+ 1 papposerrate+ 3–4 simple setae terminally; dactylus stout, apically curved, with 3 spines along
inner margin and 3–4 simple setae; exopod absent.
Pleon (Fig. 6A): 6 somites, pleomeres with broadly rounded posteroventral margins; fourth, fifth and sixth
pleomeres with simple setae, distributed as illustrated.
Pleopods (Fig. 6O–S): functional; well developed, biramous; protopod naked except in fourth and fifth
pleopods where it bears 1 plumose seta distally on inner margin; first pleopod endopod with 3 plumose setae and
exopod with 7 plumose setae distributed as figured; second and third pleopods bearing endopods with 6 and 8
plumose setae respectively and exopods of both pleopods with 8 plumose setae, distributed as figured; fourth and
fifth pleopods bearing endopods with 8 and 7 plumose setae respectively and exopods with 8 and 10 plumose setae
respectively, distributed as figured, epipods present in both pleopods with 2 cincinulli.
Uropods (Fig. 6T): protopod unarmed; endopod with 4–5 short sparsely plumose setae proximally on outer
margin, 20–21 plumose setae along distal and inner margins, and 5–6 plumose setae on dorsal margin; exopod with
8 short sparsely plumose setae on outer margin+ 1 spine on apex followed by 25–26 marginal plumose setae, and
2–3 simple setae on dorsal distal margin.
Telson (Fig. 6T, T’): bears 2 pairs of short lateral spines followed by 4 pairs of processes distally (the first pair
of spines are the shortest, the second pair of spines are the longest, the third pair of processes are long simple setae,
and the fourth inner pair of processes are strong plumose setae).
Discussion
The complete larval development of Thor amboinensis presents the same number of stages as T. floridanus (Broad
1957): eight zoeae and one decapodid. Both species have a similar sequence of appearance of characters, but they
are easily distinguished. The first zoeal stage of T. floridanus presents three denticles in the ventral margin of the
carapace, absent in T. amboinensis. In the second zoeal stage the differences in the carapace persist, with T.
floridanus presenting an antennal spine. The most obvious difference between the two species appears from the
fifth stage on in the pereiopods development: T. floridanus presents the third pereiopod as a uniramous bud and T.
amboinensis has the third pereiopod as a biramous bud. In the last zoeal stage T. floridanus will have pereiopods
three to five uniramous, while T. amboinensis has the fourth and fifth pereiopods uniramous, a variation of
characters not unique in the Hippolytidae, previously noticed for different species of Eualus (Haynes 1985, Terossi
et al. 2010). Curiously, the sequence of the development of the outer flagellum of the antennule of T. amboinensis
(present study) and T. floridanus (Broad 1957) is quite peculiar. In the second to the third zoeal stage, the number
of aesthetascs in both species decreases to two, number that is kept in the fourth zoea, increasing in the fifth zoea
when the outer flagellum of the antennule presents 3 aesthetascs and 2 plumose setae.
Comparing T. amboinensis (present study) and T. floridanus (Broad 1957) larval descriptions, both with eight
zoeal stages, with the one presented by Lebour (1940), we can conclude that the identity of the species of Thor
described in 1940 remains uncertain as the larval development is shorter. The hippolytid species sensu De Grave &
Fransen (2011) usually have five to eleven stages, while those with an abbreviated development can have two to
four (Terossi et al. 2010, page 51, table 1). In the particular case of Thor, Dobkin (1968) described an abbreviated
development for Thor dobkini with two zoeal stages and a decapodid, not comparable with the one from present
study or with that described by Lebour (1940) or Broad (1957), since the more advanced morphological characters
in an abbreviated development are kept through the larval series, meaning that a first zoeal stage with the first to
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fifth pereiopods present as rudimentary structures (e.g. Thor dobkini) or with more than 7 pairs of setae on telson
(e.g. Lebbeus polaris), will need less stages to complete their development (Terossi et al. 2010, page 51, table 1).
Considering the pleopods development for example, are as small buds in Lebour’s fourth zoeal stage, but in present
study and in Broad’s description these will only appear in the sixth stage. Broad (1957) discussed the differences
found from Lebour’s (1940) description, concluding that the larvae differed in size, color, as well as in the number
and morphology of the larval stages. Broad presented two explanations for the observations made, or the larvae
belonged to different taxonomic groups, or the larvae were the same species but their development varied with the
geographic location or with other external factors. Besides, Lebour (1940) decided to keep the species identity of
the juvenile described by her undetermined, since it presented a rostrum without spines, not matching the rostrum
of the juvenile presented by Verril (1922) with three spines. In fact, Verril (1922) described T. floridanus.
Thor amboinensis is a species with a circum-tropical distribution, and caridean larvae are known as having a
high morphological plasticity (Anger 2001), with intraspecific larval morphological variations occurring between
geographic areas (e.g. Wehrtmann & Albornoz 2003). For this reason, we carefully compared the first zoeal stage
described in present study hatched from females collected in the Philippines, with that described by Yang & Okuno
(2004) from females collected in Japan. Both first zoeae are remarkably similar, however the zoeae from the
Philippines are bigger (CL
Philippin es
= 0.53–0.65 mm, CL
Japan
= 0.40–0.43 mm) and have a 5-segmented antennal scale;
also, the coxal endite of the maxillule and maxilla in our larvae have 6 and 8 setae respectively, while in Yang &
Okuno’s (2004) study the larvae have a 6-segmented antennal scale, and, 5 and 6 setae correspondingly. The
morphological similarity between the larvae from the Philippines and Japan does not reflect the morphological
plasticity described for caridean shrimp larvae (Anger 2001). Even not knowing the exact collection sites, we
might suppose that the different larval sizes at hatching could be a consequence of the water temperature, since it is
a key factor for decapod larvae development (Anger 2001); although, it would be expected to have larger larvae in
Japan, since for carideans a latitudinal pattern is observable in reproductive traits with an increase towards the
poles in larval size (e.g. Anger 2001, Thatje et al. 2003). Also the trans-generational maternal effects can be
pointed out as the reason for the newly hatched larval size differences (e.g. Giménez 2006), so we can suppose that
the well established commercial culture techniques of the ovigerous females with constant environmental
conditions resulted in an increment of eggs, variation that can be propagated to the larval stages, resulting in higher
biomass at hatching. In the future, in order to understand the influence of the water temperature in the larval size, as
well as to verify the conservative morphology of the newly hatched larvae of T. amboinensis, other populations
from different geographical areas of the range of distribution of this species, such as the western (e.g. Caribbean)
and the eastern Atlantic (e.g. Madeira), should be considered.
Together with the morphometric and morphological comparison of the adults and larvae of T. am b oinen s i s,
also the genetic analysis of the different populations would be extremely helpful to clarify some of the results
obtained by the phylogenetic reconstruction of the family Thoridae presented in this study. In fact, the COI
pairwise distances between the considered populations of T. amboinensis suggest cryptic speciation for
geographical separated populations, given that the minimum distance between populations of this species is 6.8 %
(between the Philippines and Moorea), a value superior to what is accepted for COI distances within a species
(Lefébure et al. 2006, Costa et al. 2007, Radulovici et al. 2009). Therefore, to clarify the circum-tropical species
complex of Thor amboinensis, the inclusion of the population of the type locality (Amboina, Molucas Sea) in
future studies using COI as molecular marker will be valued (e.g. Puillandre et al. 2011). Another evident result is
the paraphyly of genus Eualus as suggested before (Costa et al. 2007, De Grave et al. 2014), and the positioning of
Eualus cranchii grouped together with the specimens of T. amboinensis with a high branch support. As De Grave et
al. (2014) suggested the genus Eualus needs to be carefully checked, and E. cranchii needs to be reassigned to a
different genus, most probably Thoralus. In order to verify the sister clade relationship between Thinora and Thor,
it would be very valuable to include in the COI gene phylogeny their representatives.
Sarver (1979) described in his paper the larval culture of T. amboinensis, but he does not give any information
about the morphology of the stages obtained. In fact that was not his objective. However, the author referred that
the larvae were reared for 6 weeks, passing through 10 to 12 stages, numbers that are not coincident with what was
obtained in present study where after 28 days the metamorphosis from the eighth zoeal stage to the decapodid
occurred. Most probably, as the author supposed in his discussion (Sarver 1979), the larvae entered in mark time
molting (defined by Gore 1985).
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The lack of knowledge for the genus Thor, as well as the variability of the results considering the number of
zoeal stages obtained by previous authors makes us to be very careful in the establishment of the general
morphological features of the larvae of the genus. Even so, we consider that the zoeae of Thor beyond the first
zoeal stage present: a rostrum triangular, broad and short, reaching a maximum length correspondent to half of the
eye; the carapace has anterior and posterior dorsomedian papillae as well as anteroventral denticle(s); no
mandibular palp through all development; the third pleomere distinctly curved and all pleomeres without spines;
the pereiopods three to five or four to five are uniramous.
The taxonomy of the family Hippolytidae sensu De Grave & Fransen (2011) is not established, and De Grave
et al. (2014) based on molecular results proposed a new classification for it, resurrecting family Thoridae Kingsley,
1879, since a strong nodal support was found for some of the genera included in the study. According to the
authors, genera Birulia, Eualus, Heptacarpus, Lebbeus, Paralebbeus, Spirontocaris, Thinora and Thor should be
together in family Thoridae. Considering the larvae, some of the referred genera were already discussed in the past
(e.g. Gurney 1937, Pike & Williamson 1961, Haynes 1985, Terossi et al. 2010), and in general the diagnosing
larval characters signed by the authors for the different genera agree well with the grouping of genera in Thoridae,
supporting it from a larval morphology perspective. Taking into account present results together with those from
previous authors, we can consider that the larval characters for family Thoridae Kingsley, 1879 are: nine zoeal
stages and one decapodid; rostrum absent to long (reaching the end of the antennular peduncle), usually without
spines; the eyestalks are almost cylindrical, and not long; the antennular peduncles are straight; the basis of the
maxillule does not present a subterminal seta; the pereiopods are more or less equal in size, and the exopods are
present on pereiopods 1 to 2, 1 to 3 or 1 to 4; whenever present the posterolateral spines are on pleomeres 4 and/ or
5. Future research needs to be done, to complete the larval development of the different species of Thor adding
more information about the development of the genus, as well as to obtain at least the newly hatched zoea for those
genera for whom the larval development remains unknown (Birulia, Paralebbeus and Thinora), confirming the
larval characters proposed by present study for the recently resurrected family Thoridae.
Acknowledgements
The authors would like to thank to Lusoreef- Criação de Espécies Marinhas, Lda. for all the rearing techniques
support. Special thanks to Dr. Helena Costa that kindly made available the laboratory facilities in Faculdade de
Ciências e Tecnologia, Universidade Nova de Lisboa, where the molecular work was developed, and to Jorge Lobo
who helped with the extraction and amplification protocols. The molecular identification of the specimens was
funded by the Fundação para a Ciência e a Tecnologia (FCT), research project “LusoMarBol- Lusitanian Marine
Barcode of Life” (POCTI/1999/BSE/36663), coordinated by Filipe O. Costa. CB is supported by Fundação para a
Ciência e a Tecnologia (FCT) through the postdoctoral fellowship SFRH/BPD/63888/2009. The specimens used by
present study were collected and reared under appropriate permits and approved ethics guidelines. The comments
of two anonymous reviewers improved the quality of this manuscript.
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