Variable microsatellite markers for a snapping shrimp (Alpheus armillatus) species complex

Snapping shrimp (Alpheus) are an important ecological component of tropical marine systems and are excellent models for studies of phylogeography and behavioural ecology. Here, I describe 10 variable microsatellite loci for the Alpheus armillatus species complex of snapping shrimp. The primers were tested on 60 individuals representing three evolutionary lineages within the complex, and yielded three to 21 alleles. These loci will be effective tools in future studies on population genetics and mating behaviour in this complex.     

Post-autotomy claw regrowth and functional recovery in the snapping shrimp Alpheus angulosus

The ability to regenerate lost tissues, organs or whole body parts is widespread across animal taxa; in some animals, regeneration includes transforming a remaining structure to replace the one that was lost. The transformation of one limb into another involves considerable plasticity in morphology, physiology and behavior, and snapping shrimp offer excellent opportunities for studying this process. We examined the changes required for the transformation of the small pincer to a mature snapping claw in Alpheus angulosus. First molt claws differ from mature claws in overall shape as well as in morphology related to snapping function; nonetheless, shrimp with first molt claws do produce snaps. While most shape variables of second molt claws do not differ significantly from mature claws, the plunger (structure required for snap production) does not reach mature size until the third molt for females, or later for males. Thus, the pincer claw can be transformed into a functional snapping claw in one molt, although both the underlying morphology and superficial shape are not fully regenerated at this stage. The rapid production of a functional snapping claw that we observe in this study suggests that this particular function is of significant importance to snapping shrimp behavior and survival.     

Individual discrimination in the big-clawed snapping shrimp, Alpheus heterochelis

Rahman et al. (Rahman, N., Dunham, D.W. and Govind, C.K. (2001). Mate recognition and pairing in the big-clawed snapping shrimp, Alpheus herterochelis. Mar. Fresh. Behav. Physiol., 34, 213-226.) demonstrated discrimination by snapping shrimp between former mates and unfamiliar conspecifics, but did not test individual discrimination. In the present study, snapping shrimp showed discrimination between familiar and unfamiliar same-sex conspecifics by preferentially entering that arm of a Y-maze leading to familiar individuals. Furthermore, after being exposed to water from the home tanks of unknown individuals, they later showed an elevated response to this water, if the direction from which the water came into their tank was changed to be novel. This indicates that test subjects associated a familiar chemical stimulus with its location in the environment. This discrimination could only have been made if that chemical signature were recognised as different from that of another chemically familiar individual. This result also demonstrates that the water surrounding an individual contains sufficient (chemical) information to allow discrimination of one individual from another.     

Individual discrimination in the big-clawed snapping shrimp,Alpheus heterochelis

Rahman et al. (Rahman, N., Dunham, D.W. and Govind, C.K. (). Mate recognition and pairing in the big-clawed snapping shrimp, Alpheus herterochelis. Mar. Fresh. Behav. Physiol., 34, 213–226.) demonstrated discrimination by snapping shrimp between former mates and unfamiliar conspecifics, but did not test individual discrimination. In the present study, snapping shrimp showed discrimination between familiar and unfamiliar same-sex conspecifics by preferentially entering that arm of a Y-maze leading to familiar individuals. Furthermore, after being exposed to water from the home tanks of unknown individuals, they later showed an elevated response to this water, if the direction from which the water came into their tank was changed to be novel. This indicates that test subjects associated a familiar chemical stimulus with its location in the environment. This discrimination could only have been made if that chemical signature were recognised as different from that of another chemically familiar individual. This result also demonstrates that the water surrounding an individual contains sufficient (chemical) information to allow discrimination of one individual from another.     

Larval,megalopal and early juvenile development in Pagurus granosimanus (Stimpson, 1859) (Decapoda: Anomura: Paguridae) reared in the laboratory

Summary

The larval, megalopal and early juvenile stages of Pagurus granosimanus are described, illustrated and compared with other North Pacific species of the genus. Morphologically, the zoeae of P. granosimanus appear most similar to the Japanese P. brachiomastus in the majority of characters, but share the endopodal setation of the third maxilliped with a second Japanese species, P. pectinatus. The megalopae of P. granosimanus are unlike those of other North Pacific species in having 5+5 marginal setae on the telson, rather than the customary 4+4, or less frequent 3+3. Comparison of juvenile characters is limited to pleopodal changes among the regional species for which data are available. P. granosimanus is unusual in undergoing complete pleopodal loss at the second crab stage with return of left pleopods in the fourth stage.     

Snapping behaviour in intraspecific agonistic encounters in the snapping shrimp (Alpheus heterochaelis)

During intraspecific agonistic encounters in snapping shrimp (Alpheus heterochaelis) the behaviour of the snapper, emitting a fast water jet by very rapid closure of the large modified snapper claw, and the receiver was analysed by single frame video analysis before, during, and after the snap. During snapping the opponents usually face each other. Snapping is most frequently preceded by touch of frontal appendages. The snapping animal keeps its snapper claw slightly across the midline, shielding frontal body parts, and its tailfan bent downwards. The mean claw cocking duration (generating muscle tension) before snapping amounts to about 500 ms. In 58% of the snaps, the snapper claw pointed at the opponent, its claws, densely covered with sensory hairs, representing the main target of the water jet. The mean distance for these directed snaps was 0.9 cm, while undirected snaps were emitted from larger distances of on average 3.4 cm. The snapper usually withdraws immediately after snapping, the receiver approaches. Initial snaps are often answered by return snaps and both are emitted from smaller distances and hit more often than subsequent snaps.     

Complete mitochondrial genome of the Japanese snapping shrimp Alpheus japonicus (Crustacea: Decapoda: Caridea): Gene rearrangement and phylogeny within Caridea

The complete sequence of the mitochondrial genome of the Japanese snapping shrimp Alpheus japonicus Miers (Crustacea: Decapoda: Caridea) is presented here. A comparative analysis based on the currently available mitochondrial genomic data revealed many previously unknown characteristics of the mitochondrial genomes of caridean shrimps. The A. japonicus mitochondrial genome is 16487 bp long and contains the typical set of 37 metazoan genes. The gene arrangements in the mitochondrial genomes of four previously studied carideans (Macrobrachium rosenbergii, M. nipponense, M. lanchesteri and Halocaridina rubra) were found to be identical to the pancrustacean ground pattern; thus, it was considered that gene rearrangements probably did not occur in the suborder Caridea. In the present study, a translocation of the trnE gene involving inversion was found in Alpheus mitochondrial genomes. This phenomenon has not been reported in any other crustacean mitochondrial genome that has been studied so far; however, the translocation of one transfer RNA gene (trnP or trnT) was reported in the mitochondrial genome of Exopalaemon carinicauda. When the ratios of the nonsynonymous and synonymous substitutions rates (Ka/Ks) for the 13 protein coding genes from two Alpheus species (A. japonicus and A. distinguendus) and three Macrobrachium species (M. rosenbergii, M. nipponense, M. lanchesteri) were calculated, the Ka/Ks values for all the protein coding genes in Alpheus and Macrobrachium mitochondrial genomes were found to be less than 1 (between 0.0048 and 0.2057), indicating that a strong purification selection had occurred. The phylogenetic tree that was constructed based on the mitochondrial protein coding genes in the genomes of nine related species indicated that Palaemonidae and Alpheidae formed a monophyly and shared a statistically significant relationship, (Palaemonidae+Alpheidae)+Atyidae, at the family level.     

Population structure,relative growth and morphological sexual maturity of the snapping shrimp Alpheus brasileiro Anker, 2012 (Caridea: Alpheidae) from the south-eastern coast of Brazil

The present study investigated the population structure of the snapping shrimp Alpheus brasileiro. We tested the hypotheses that the sex ratio of the population differs from the expected 1:1 and that the growth pattern differs between adults and juveniles and between sexes. Reproductive period, juvenile recruitment and morphological sexual maturity were estimated. Samples were collected in two periods. The first sampling occurred bimonthly from March 2013 to January 2014. The second sampling occurred monthly from April 2015 to March 2016. The population structure was determined based on the size-frequency distribution of different demographic categories. To analyse the relative growth, we measured the second pleuron length, major cheliped propodus length, major cheliped propodus width, major cheliped propodus height, appendix interna length, appendix masculina length. The results showed that the sex ratio did not differ from 1:1 (male:female). Reproduction and juvenile recruitment were continuous throughout the study period. The analysis of relative growth confirmed the hypothesis that males and females, and juveniles and adults, have different growth patterns, indicating distinct strategies of energy allocation. The estimated carapace length at the onset of morphological sexual maturity was 4.9?mm in males and 4.7?mm in females. The results obtained in this study are probably related to the monogamous social behaviour of A. brasileiro. Monogamy can influence demographic parameters such as sex ratio and the size at which males and females reach morphological sexual maturity.     

Correct diagnosis of early zoeal stages of Athanas nitescens (Leach, 1814) (Decapoda, Caridea, Alpheidae) using laboratory-raised larvae

The morphology of the first two larval stages of Athanas nitescens(Leach, 1814), reared under laboratory conditions, is redescribed.The present data are compared with previous works, since a clarificationof the morphological characters of the first two larval stagesof A. nitescens is needed, in order to avoid misidentificationof these stages in the future.     

Flow visualisation and high speed video analysis of water jets in the snapping shrimp (Alpheus heterochaelis)

Snapping shrimp (Alpheus heterochaelis) produce a fast, well-focused water jet by rapid closure of their specialised snapper claw. As shown previously, water jets may injure the opponent in interspecific encounters (e.g. with small crabs) although no damage was observed in intraspecific encounters. For conspecific receivers the jet represents a potential hydrodynamic signal and can be analysed with the help of mechanosensory hairs. To gain more insight in the biophysical characteristics of the water jet we visualised and analysed jets of tethered snapping shrimp using standard and high speed video recordings. Water jet width increases with increasing distance from the snapper claw tip, and both width and distance increase with increasing snapper claw size. Water jet distances do not increase with increasing claw cocking duration (building up muscle tension) but medium cocking durations of about 550 ms result in longest distances. Mean water jet velocity is 6.5 m s⁻¹ shortly after claw closure but rapidly decreases subsequently. At the mean distance between snapping conspecifics (9 mm) water jet velocities produced by snapping shrimp with larger snapper claws are significantly higher than those of animals with smaller claws. Interestingly, males with equal snapper claw size as females produce significantly faster water jets. Accepted: 31 March 1999     

Morphology of prezoea in the porcelain crab <Emphasis Type="Italic">Pachycheles stevensii</Emphasis> (Decapoda: Anomura: Porcellanidae) reared under laboratory conditions

Pachycheles stevensii Stimpson, 1858 is the only species of the family Porcellanidae (Decapoda, Anomura) living in the Russian waters of the Sea of Japan. The morphology of prezoeal larval stages of this crab obtained under laboratory conditions for the first time was studied and described in detail.Original Russian Text Copyright © 2005 by Biologiya Morya, Kornienko.     

Deception with honest signals: signal residuals and signal function in snapping shrimp

Animals in competitive interactions often assess the competitiveability of opponents using signals. Signals used in competitiveinteractions are generally predicted to be honest, but opento low levels of deceit. Such "incomplete honesty" in signalscan be studied by using signal residuals, the residuals fromthe regression of a measure of signal structure on competitiveability. Specifically, individuals with positive signal residualsproduce signals that exaggerate their competitive ability; deceptive use of these signals may occur if signalers for whom the signalexaggerates their apparent competitive ability use the signalmore frequently. I used this framework to examine the use ofthe open chela display by big-clawed snapping shrimp (Alpheusheterochaelis). Competitive interactions between snapping shrimpare resolved primarily on the basis of body size, and the open chela display is used by males to assess body size. I foundthat the production of the open chela display by males respondingto superior competitors depends on chela residuals, such thatindividuals for whom the display exaggerates their apparentsize produce the display more often. This effect can be seenboth in response to isolated chelae and in staged competitiveinteractions. Interactions involving shrimp with larger chela residuals are long and highly escalated, suggesting that chelaresiduals affect assessment of competitive ability. Thus, theincreased use of the open chela display by males for whichthe display exaggerates apparent body size is an example ofdeceptive use of an otherwise honest signal.     

Antifouling adaptations of marine shrimp (Decapoda: Caridea): gill cleaning mechanisms and grooming of brooded embryos

Gills in the branchial chambers of caridean shrimps, as well as the brooded embryos in females, are subject to fouling by particulate debris and epizoites. Important mechanisms for cleaning the gills are brushing of the gills by the grooming or cleaning chelipeds in some species, while in others, setae from the bases of the thoracic legs brush up among the gills during movement of the limbs (epipodsetobranch complexes). Setae of cleaning chelipeds and of epipod-setobranch complexes show similar ultrastructural adaptions for scraping gill surfaces. Ablation of the cleaning chelipeds of the shrimp Heptacarpus pictus results in severe fouling of the gills in experimentals, while those of controls remain clean. Embryos brooded by female carideans are often brushed and jostled by the grooming chelipeds. In H. pictus , removal of the cleaning chelae results in heavier microbial and sediment fouling than in controls.     

Tests of the mate-guarding hypothesis for social monogamy: male snapping shrimp prefer to associate with high-value females

Social monogamy without biparental care has evolved in manytaxa, and a number of hypotheses have been developed to explainthis phenomenon. Several authors have suggested the importanceof male mate-guarding behavior in the evolution of social monogamy,although empirical support for this hypothesis is lacking. Inthe caridean shrimp genus Alpheus, social monogamy may resultfrom selection on males for long-term guarding of females becausemating is temporally restricted to a short time after the female'smolt. I used Alpheus angulatus to test two predictions of theextended mate-guarding hypothesis: Males should (1) be physiologicallycapable of predicting the timing of female sexual receptivity,and (2) prefer to associate with (guard) females that are closerto sexual receptivity. Data from a Y-maze experiment testingfor distance chemical communication showed that males of A.angulatus were attracted to water treated by exposure to premoltfemales, repulsed by water treated by exposure to intermoltmales and females, and did not appear to respond in either directionto water treated by exposure to premolt males. In mate choiceexperiments, significantly more males paired with premolt femalesthan with postmolt females. These data suggest that males ofA. angulatus engage in precopulatory mate-guarding behavior.Other factors (population density, sex ratio) may have playeda role in the temporal extension of mate guarding to socialmonogamy.     

Molecular phylogeny reveals extensive ancient and ongoing radiations in a snapping shrimp species complex (Crustacea,Alpheidae, Alpheus armillatus)

Tropical marine habitats often harbor high biodiversity, including many cryptic taxa. Though the prevalence of cryptic marine taxa is well known, the evolutionary histories of these groups remain poorly understood. The snapping shrimp genus Alpheus is a good model for such investigations, as cryptic species complexes are very common, indicating widespread genetic diversification with little or no morphological change. Here, we present an extensive phylogeographic investigation of the diversified amphi-American Alpheus armillatus species complex, with geographic sampling in the Caribbean Sea, Gulf of Mexico, Florida, Brazil, and the tropical Eastern Pacific. Sequence data from two mitochondrial genes (16SrRNA and cytochrome oxidase I) and one nuclear gene (myosin heavy chain) provide strong evidence for division of the species complex into six major clades, with extensive substructure within each clade. Our total data set suggests that the A. armillatus complex includes no less than 19 putative divergent lineages, 11 in the Western Atlantic and 8 in the Eastern Pacific. Estimates of divergence times from Bayesian analyses indicate that the radiation of the species complex began ～10 MYA with the most recent divergences among subclades dating to within the last 3 MY. Furthermore, individuals from the six major clades had broadly overlapping geographic distributions, which may reflect secondary contact among previously isolated lineages, and have apparently undergone several changes in superficial coloration, which is typically the most pronounced phenotypic character distinguishing lineages. In addition, the extensive substructure within clades indicates a great deal of molecular diversification following the rise of the Isthmus of Panama. In summary, this investigation reflects substantial biodiversity concealed by morphological similarity, and suggests that both ancient and ongoing divergences have contributed to the generation of this biodiversity. It also underlines the necessity to work with the most complete data set possible, which includes comprehensive and wide-ranging sampling of taxa.     

Microsatellite development suggests evidence of polyploidy in the social sponge-dwelling snapping shrimp Zuzalpheus brooksi

We isolated and characterized 33 novel, polymorphic microsatellite loci from the social sponge‐dwelling snapping shrimp Zuzalpheus brooksi. We screened all 33 loci in approximately 31 individuals from a population of Z. brooksi from the Florida Keys, USA and found an average of 16 alleles per locus. Approximately 25% of the loci showed more than two bands per individual, suggesting evidence of high gene duplication, or more likely, polyploidy, which is common in crustaceans. The 25 disomic loci had an observed heterozygosity of 0.57 (range = 0.03–1.00) and will be useful for studying the social organization in Zuzalpheus shrimp.     

Visual orientation of the symbiotic snapping shrimp Synalpheus demani

Visual cues play an important role in crustacean shelter-seeking behavior. We hypothesize that Synalpheus demani, an obligate crinoid-dwelling snapping shrimp, uses visual cues in host location. We tested shrimp response to rectangular visual targets that subtended 10°, 30°, 90°, 180°, and 270° in a circular arena in background seawater and in seawater containing host odor. In background seawater, S. demani oriented to solid visual targets of 90° and larger, and avoided the 10° and 30° target. Orientation to targets is interpreted as refuge-seeking behavior. Avoidance is speculated as predator-avoidance behavior. Shrimp oriented to large visual targets in sea water and host odor. The presence of host odor altered avoidance responses of a significant number, but not all, shrimp to small targets. Host odor also increased shrimp activities in the arena. Synalpheus demani oriented to 90° patterned (vertical and horizontal stripes, and checker board) targets, but they did not orient to 270° patterned targets. This was interpreted as positive scototaxis, which is common in many crustaceans. Thus we conclude that visual orientation of S. demani is similar to that of free-living snapping shrimp.     

The zoeal stages and megalopa of Portunus rubromarginatus (Lanchester) (Decapoda: Portnnidae), reared in the laboratory

The present state of knowledge concerning Portunus larvae isreviewed, and the three zoeal and the megalopa stages of P.rubromarginatus are described and figured. Details of appendagesetation are tabulated. This species is unusual amongst knownPortunus spp. in having only three zoeal stages and, like otherPortunus spp. but in contrast with other Portuninae, it has4 + 4, or 4 + 1 + 4, setae on the posterior telson border. When compared with larvae of the five other Indo-West PacificPortunus species whose larvae are known P. rubromarginatus zoeaeare readily distinguished from all, except P. hastatoides, usingthe key features given by Kurata (1975). Comparison was madebetween first zoeae of these two species, and also of P. pelagicusand P. sanguinolentus, using larvae reared by the authors. Itwas found telson characters alone allow distinction betweenlarvae of these four species. These characters are tabulated. P. rubromarginatus megalopae differ from those known for congenitorsin having a large spine on the uchium of the first pereiopod,but not on the carpus, and in having relatively very small sternalcornuae. Several of these features disagree with those previously thoughtto characterise larval Portuninae or Portunus species.     

Signaling via water currents in behavioral interactions of snapping shrimp (Alpheus heterochaelis)

The snappping shrimp Alpheus heterochaelis produces a variety of different water currents during intraspecific encounters and interspecific interactions with small sympatric crabs (Eurypanopeus depressus). We studied the mechanisms of current production in tethered shrimp and the use of the different currents in freely behaving animals. The beating of the pleopods results in strong posteriorly directed currents. Although they reach rather far, these currents show no distinctions when directed toward different opponents. Gill currents are produced by movements of the scaphognathites (the exopodites of the second maxillae) and can then be deflected laterally by movements of the exopodites of the first and second maxillipeds. These frequent but slow lateral gill currents are most probably used to enhance chemical odor perception. The fast and focused, anteriorly directed gill currents, however, represent a powerful tool in intraspecific signaling, because they reach the chemo- and mechanosensory antennules of the opponent more often than any other currents and also because they are produced soon after previous contacts between the animals. They may carry chemical information about the social status of their producers since dominant shrimp release more anterior gill currents and more water jets than subordinate animals in intrasexual interactions.     

Egg production, hatching rates, and abbreviated larval development of Campylonotus vagans Bate, 1888 (Crustacea: Decapoda: Caridea), in subantarctic waters

Early life history patterns were studied in the caridean shrimp, Campylonotus vagans Bate, 1888, from the subantarctic Beagle Channel (Tierra del Fuego). As a consequence of very large egg size (minimum 1.4 mm), fecundity was low, ranging from 83 to 608 eggs per female (carapace length [CL] 11-22.5 mm). Egg size increased continuously throughout embryonic development, reaching prior to hatching about 175% of the initial diameter. Due to low daily numbers of larval release, hatching of an egg batch lasted for about 2-3 weeks. The complete larval and early juvenile development was studied in laboratory cultures fed with Artemia sp. nauplii. At 7.0±0.5 °C, development from hatching to metamorphosis lasted for about 6 weeks. It comprised invariably two large zoeal stages and one decapodid, with mean stage durations of 12, 17, and 15 days, respectively. Larvae maintained without food survived on average for 18 days (maximum: 29 days), but did not reach the moult to the zoea II stage. Size increments at ecdysis were low in all larval stages (2.1-3.9%), indicating partial utilisation of internal energy reserves. A clearly higher increment (14%) was observed in the moult from the first to the second juvenile stage. Low fecundity, large size of eggs and larvae, an abbreviated mode of larval development, high larval survival rates during absence of food, demersal behaviour of the early life history stages, and an extended hatching period with low daily release rates are interpreted as adaptations to conditions typically prevailing in subantarctic regions, namely low temperatures (causing long durations of development) in combination with a pronounced seasonality in plankton production (i.e., short periods of food availability).