Triops Longicaudatus Research Articles

Comparative transcriptomics suggests a potential realizator gene for carapace expansion in longtail tadpole shrimp, Triops longicaudatus (Branchiopoda: Notostraca).

The origin of morphological innovation has been extensively studied within evolutionary developmental biology (evo-devo). Recent studies have demonstrated that the developmental module for double-layered epithelial outgrowths is conserved between the insect wings and branchiopod crustacean carapace, thereby introducing homology among these diverse structures. However, evo-devo studies on the branchiopod crustacean carapace have been primarily limited to a single species, the water flea Daphnia magna, leaving the gene regulatory network governing carapace development not comprehensively understood. Furthermore, realizator genes downstream of the character identity mechanism (ChIM) for bilayered epithelial development remain inadequately described. In this study, we analyzed tissue-specific transcriptional profiles in the developing longtail tadpole shrimp, Triops longicaudatus. We observed significant upregulation of papilin in the carapace-bearing head, along with its expression in both the carapace and the trunk limb lobes. Based on these results, we hypothesize that differential expression of papilin is involved in the disproportional growth of Triops carapace. Our findings will contribute to elucidating the diversification of double-layered epithelial outgrowths across distant arthropod lineages.

Characterization of tadpole shrimp, Triops longicaudatus (Notostraca: Triopsidae), injury to rice and its effect on rice seedling establishment.

Rice seedlings of different stages of development were infested with tadpole shrimp (TPS, Triops longicaudatus [LeConte]), of different sizes in four experiments conducted in a lath house in Colusa, CA, during 2015 and 2016. Tadpole shrimp size was based on carapace length. Rice seedling stages were classified as S0 if no structures were present; S1 if only the coleoptile was present; S2 if the coleoptile and radicle were present; S3-I if the prophyll had emerged; S3-II if the first true leave had emerged but was not unfurled; and V1 if the first true leave was unfurled. Results showed that TPS of all sizes are capable of injuring rice and reducing seedling establishment, with larger TPS causing more seedling establishment reduction than medium or small TPS. The coleoptile, radicle, and roots were the structures most injured by TPS. During the S0 stage, TPS buried seeds, preventing their establishment. Seedling stages S1, S2, and S3-I were found to have the highest risk of injury by TPS, while seedling stage V1 had the lowest. Pearson's correlation between injured seedlings and the normalized number of established seedlings indicates that injury to the coleoptile, root, and radicle combined are the most important in preventing seedling establishment.

Alternative Chemical Control Options and Monitoring Techniques for Triops longicaudatus (Notostraca: Triopsidae) in California Rice.

The tadpole shrimp (Triops longicaudatus (Leconte); Notostraca; Triopsidae) is a vernal pool crustacean that has emerged as a significant pest for many rice farmers in California. Currently, lambda-cyhalothrin is the commercial standard and sole management practice for TPS, but resistance appears to be emerging. Field and laboratory trials were conducted from 2015 to 2018 at the Rice Experiment Station in Biggs, California, and in greenhouses at the University of California (UC) Davis to evaluate the efficacy of several alternative chemical controls and to explore early indicators of TPS activity and damage as monitoring tools. TPS mortality in plots treated with azadirachtin was not significantly different from those in the untreated control across all trials. Copper sulfate, lambda-cyhalothrin, and clothianidin were consistently effective across both lab and field trials. Chlorantraniliprole generated effective control in four of the five trials, whereas two diflubenzuron rates generated adequate control in the field, but not in laboratory bioassays. Thus, there appear to be several effective alternative control options available for farmers, should resistance to lambda-cyhalothrin continue to spread. Water turbidity (measured using a scale of 1-4) and the number of dislodged seedlings were both significantly correlated with TPS counts in field studies. Turbidity exhibited the highest correlations with TPS counts, suggesting that with further refinement it could play a valuable role in monitoring TPS populations.

Effect of Rice Winter Cultural Management Practices on the Size of the Hatching Population of Triops longicaudatus (Notostraca: Triopsidae) in California Rice Fields.

The tadpole shrimp [Triops longicaudatus (Leconte)] has emerged as a significant pest of rice grown in California in recent decades. The change in T. longicaudatus' pest status has coincided with changes in cultural management of residual rice straw postharvest. Policy changes have reduced the postharvest burning of fields from nearly 95% to less than 10%, promoting increased use of winter flooding as a means of accelerating straw decomposition. Field and laboratory trials were conducted from 2015 to 2017 at the Rice Experiment Station in Biggs, CA and in greenhouses at the University of California (UC) Davis to evaluate the effects of burning, flooding, and a fallow control on T. longicaudatus population dynamics. Experiments demonstrated that burning of rice straw failed to suppress densities of hatching T. longicaudatus and actually had the reverse effect, causing a 51% increase in numbers hatching, perhaps as a result of burning triggering termination of multiyear T. longicaudatus egg dormancy. Winter flooding had no measurable effect on T. longicaudatus hatch. Thus, these changes in winter cultural practices do not appear to be responsible for the emergence of T. longicaudatus as a major rice pest.

First record of Triops strenuus Wolf, 1911 (Branchiopoda, Notostraca), a tadpole shrimp of Australian origin, from Japan

Three species of tadpole shrimp, i.e.,Triops granarius(Lucas, 1864),Triops longicaudatus(LeConte, 1846) andTriops cancriformis(Bosc, 1801-1802), have been known from Japan. In this paper the author describes a fourthTriopsspecies (= Triops strenuusWolf, 1911) living in the rice paddies of a southern area of Honshu, the largest of the four main islands of Japan. This species was probably endemic to the Australian continent, and no habitat distribution outside Australia has been reported so far. The impact on the existing ecosystem of Japan is quite unknown, and therefore, it is necessary to announce this intrusion into Japan in order to clarify the invasion route, habitat ecology, and the future measures against this new alien species. This invasion is considered to be caused by the resting eggs brought together with silica sand (imported from Western Australia into Japan for the large-scale beach improvement). The results presented here also describe the phylogenetic relationship with all the Australian species described so far, but also all the knownTriopsspecies of the world, based on the nucleotide sequences of mitochondrial DNA.

Review of a New Pest of Rice, Tadpole Shrimp (Notostraca: Triopsidae), in the Midsouthern United States and a Winter Scouting Method of Rice Fields for Preplanting Detection

Tadpole shrimp, Triops longicaudatus (LeConte), are a species of temporary, freshwater habitats. Tadpole shrimp are pests of rice production systems in California and have recently been found impacting Missouri rice fields and present in northeastern Arkansas rice fields. These impacts take the form of stand reduction by direct feeding on seedlings and uprooting seedlings during foraging. In addition, their foraging behavior causes water to become muddy, which reduces light penetration to submerged seedlings and consequently delays the development of the rice plant. Once rice is past the seedling stage, tadpole shrimp may be beneficial. This article provides information on the life cycle of tadpole shrimp, describes a new method for scouting for tadpole shrimp in rice fields, and provides scouting results and management implications.

Trehalose and Vitreous States: Desiccation Tolerance of Dormant Stages of the CrustaceansTriopsandDaphnia

Several aquatic organisms are able to withstand extreme desiccation in at least one of their life stages. This is commonly known as "anhydrobiosis." It was often thought that to tolerate such a desiccated state required high amounts of compatible solutes such as the nonreducing disaccharide trehalose, which protects cellular structures by water replacement and glass formation. Trehalose levels of dormant eggs and cysts of five freshwater crustaceans (Daphnia magna, Daphnia pulex, Triops longicaudatus, Triops cancriformis, and Triops australiensis) were observed in different states of hydration and dehydration. Although trehalose was detected in all species, the concentration was under 0.5% of the dry weight (0.05 μg/μg protein), and no change between the different states was observed. Differential scanning calorimetry (DSC) measurements indicated that dried cysts of all Triops species were in a glassy state, supporting the vitrification hypothesis. No indication for a vitreous state was found in dried resting eggs of Daphnia.

R2 dynamics in Triops cancriformis (Bosc, 1801) (Crustacea, Branchiopoda, Notostraca): turnover rate and 28S concerted evolution

The R2 retrotransposon is here characterized in bisexual populations of the European crustacean Triops cancriformis. The isolated element matches well with the general aspects of the R2 family and it is highly differentiated from that of the congeneric North American Triops longicaudatus. The analysis of 5' truncations indicates that R2 dynamics in T. cancriformis populations show a high turnover rate as observed in Drosophila simulans. For the first time in the literature, though, individuals harboring truncation variants, but lacking the complete element, are found. Present results suggest that transposition-mediated deletion mechanisms, possibly involving genomic turnover processes acting on rDNAs, can dramatically decrease the copy number or even delete R2 from the ribosomal locus. The presence of R2 does not seem to impact on the nucleotide variation of inserted 28S rDNA with respect to the uninserted genes. On the other hand, a low level of polymorphism characterizes rDNA units because new 28S variants continuously spread across the ribosomal array. Again, the interplay between transposition-mediated deletion and molecular drive may explain this pattern.

A New Pest of Rice in Missouri: Range Expansion of Triops longicaudatus (Crustacea: Notostraca: Triopsidae) into the Northern Mississippi River Alluvial Plains

Tadpole shrimp, Triops longicaudatus (LeConte) (Notostraca: Triopsidae), are pests in California rice production systems. Tadpole shrimp are an obligate species of ephemeral freshwater aquatic habitats and in North America were considered primarily a species of the western United State for many years. Taylor et al. (1987) reported an eastward range expansion into Oklahoma. Tadpole shrimp were not known to be in Missouri until 1979 when a report was filed with the Missouri Department of Conservation. There were 2 more records filed in 1983 and 2007. Early reports were along the Missouri River with the 1979 and 1983 reports being from Jackass Bend (Jackson County) and the 2007 record from Darst Bottoms (St. Charles County) (Dorothy Butler, personal communication). Additional populations of tadpole shrimp have been found in 2009 on the Arkansas/Missouri state line north of Gosnell, AR in Missouri (Dunklin County) and near Luxora, AR (Mississippi County). How tadpole shrimp came to be in Missouri is unknown, but dispersal occurs via floodwaters (Taylor et al. 1987), wind (Caceres & Soluk 2002; Nathan et al. 2005; Graham & Wirth 2008), birds (Green & Figuerola 2005), and via the pet trade (Halliday 2008). On June 8, 2007, a single specimen of an unknown invertebrate was brought to the Delta Research Center in Portageville, Missouri (Pemiscot County) for identification. The specimen was collected from a drill-seeded rice field in Pemiscot County (near Bakerville). The specimen was determined to be a tadpole shrimp but the species was not determined. Growers were alerted of its presence in the state at winter meetings. On May 20, 2008, a phone call was received about a 16-hectare field in Stoddard County (located north and west of Catron), of water-seeded hybrid rice that had not emerged. The water was drained from the field and thousands of tadpole shrimp were congregated in the remaining puddles. No viable seeds were present and the field was replanted (Ottis, personal observation). On June 2, 2008, another call was received about multiple fields in New Madrid County (near Lilbourn) that were infested. At least 1600 hectares had tadpole shrimp present and of those infested, nearly 800 hectares were economically impacted and approximately 40 hectares were replanted (Minson, personal observation). Specimens collected from both locations in 2008 were yellow-brown in color and 35 body segments. Two tails extended from the telson. The taxonomic treat-

Molecular Characterization of Visual Pigments in Branchiopoda and the Evolution of Opsins in Arthropoda

Studies on color vision in invertebrates have focused primarily on insect visual pigments, with little attention given to crustacean visual pigments. None of the blue-green-, blue-, or ultraviolet (UV)-sensitive-opsins have been identified in crustaceans. In addition, the discussion of visual pigments has been limited to long-wavelength-sensitive opsins in Pancrustacea. Here, we focused on Branchiopoda (Crustacea), which is a sister group of Hexapoda including insects. In the tadpole shrimp Triops granarius, the visual pigment chromophore was retinal. Multiple opsins were isolated from each of three branchiopod species, T. granarius, Triops longicaudatus, and the fairy shrimp Branchinella kugenumaensis (five, five, and four opsins from these species, respectively). Phylogenetic analyses and the presence of a lysine residue corresponding to position 90 in bovine rhodopsin suggested that three of the branchiopod opsins comprise UV-sensitive pigments. In addition, the phylogenetic relationships between insect and branchiopod UV-sensitive opsins revealed that the divergence of blue- and UV-sensitive pigments predates the Branchiopoda and Insecta divergence. The other branchiopod opsins show distant relationships to other known insect opsins and form novel clusters. The present results strongly suggest that the ancestral arthropod of the Chelicerata-Pancrustacea lineages possessed at least four types of opsins. The ancestors of Pancrustacea and the Insecta-Branchiopoda lineages possessed at least five and six types of opsins, respectively. Our results suggest that in the evolutionary process associated with each lineage, several opsins appeared and diversified with repeated gene duplication, of which some have been lost in some taxa.

Inhibition of ovarian development by methyl farnesoate in the tadpole shrimp, Triops longicaudatus

Methyl farnesoate (MF), a putative crustacean hormone, is the immediate precursor of insect juvenile hormone III (JHIII) in the biosynthetic pathway. We examined whether MF, shown to inhibit adult metamorphosis in several crustacean species, is a juvenilizing factor in the tadpole shrimp, Triops longicaudatus. Oocyte production was chosen as a parameter for measuring reproductive development. MF was administered to juveniles by ingestion via biological vector ( Artemia nauplii), MF-coated food pellets, and MF liposome food pellets. Artemia were incubated in 30 μl of 5 μg/ml MF. The MF-coated and MF liposome pellets were prepared with MF concentrations ranging between 0.1 μg/g and 10 μg/g MF by weight. Groups of tadpole shrimp were treated with these vectors from the time of hatching for 5 or 10 days in laboratory and field studies. The treatment groups of all the MF vectors showed reductions in oocyte production. Lower concentrations of MF (0.75 μg/g–3.8 μg/g MF) appeared to have a physiological effect on fecundity, but higher concentrations (10 μg/g MF) reduced somatic growth. MF-coated pellets (1 μg/g MF) administered to adults (after 5 days) caused no difference in oocyte production. The observed reductions of fecundity and the disparity of results between MF treatment on juveniles and adults suggest that MF may regulate ovarian development.

Environmental hypoxia influences hemoglobin subunit composition in the branchiopod crustaceanTriops longicaudatus

Hemoglobin (Hb) is a highly conserved protein that provides a vital link between environmental oxygen and its use and/or storage within an organism. While ubiquitous among vertebrates, Hb occurs frequently in invertebrate phyla as well. Many arthropod species use the copper-binding pigment hemocyanin, but unique in this phylum are the branchiopod crustaceans, which express Hb. Branchiopod Hb concentration and structure are exquisitely sensitive to environmental oxygen availability. Hemoglobin concentration and oxygen-binding affinity increase with decreasing oxygen tension in Daphnia, Artemia and Triops. The change in binding affinity is attributed to differential Hb subunit expression in Daphnia and Artemia but remains unclear for Triops. This is the first study to demonstrate developmental plasticity of Hb subunit expression in a notostracan, Triops longicaudatus, reared under conditions of varying oxygen availability. In response to variable oxygen environments, T. longicaudatus differentially express four primary Hb subunits ranging between 30 and 34 kDa, with normoxic-reared animals expressing primarily the heavier subunits, and hypoxic-reared animals expressing increased proportions of the lower molecular mass subunits. Moreover, differential Hb subunit expression is induced upon transfer of normoxic-reared adults to a hypoxic environment, such that the distribution of Hb subunits in the transferred adults becomes similar to that of hypoxic-reared animals. Two-dimensional gel electrophoresis and follow-up analyses revealed several isoforms of Hb subunits that may represent differential gene expression and/or post-translational modification. Unlike Daphnia and Artemia, the Hb hypoxic response in Triops is not reversible in that there was no significant decrease in Hb concentration or change in Hb subunit expression pattern when hypoxic-reared adults were transferred to a normoxic environment.

Survey of large branchiopods on Aruba and observations on taxonomic characters in Leptestheria (Spinicaudata)

A survey of more than 60 ephemeral pools during March 1989 resulted in finding three large branchiopods not previously known to occur on the Caribbean Island of Aruba. These were two Anostraca, Dendrocephalus spartaenovae Margalef, 1967 and Thamnocephalus venezuelensis Belk & Pereira, 1982, and one Spinicaudata, Leptestheria venezuelica Daday, 1923. The notostracan previously reported from Aruba, Triops longicaudatus (LeConte, 1846), was also collected from several pools. All of these species occur also in Venezuela, which is separated from Aruba by an ocean gap of about 25 km. Comparison of Leptestheria venezuelica with Leptestheria compleximanus (Packard, 1877) demonstrated that cephalic morphology provides useful taxonomic features including length of rostrum, depth of occipital notch, shape of the occipital region, and protrusion of the eye capsule. These features may prove useful in studying other species of Leptestheria.

Effect of water pH on the survival rate of larvae of the American tadpole shrimp, Triops longicaudatus (LeConte) (Notostraca : Triopsidae).

Survivorship of the larvae of American tadpole shrimp, Triops longicaudatus, was examined in the paddy water of organic farming soil which was adjusted to different pH values by NaOH solution. Among the range of pH 4.4 to 5.3, all inoculated larvae died within 12 h. In the range of pH 5.9 to 6.6, the survival rate of the larvae until 24 h was more than 50% and the rate increased with increasing pH. The effect of rectifying the acidity of organic farming paddy soil by adding Ca(OH)2 was examined in artificial paddy containers. The water pH without Ca(OH)2 was 4.9 during the first 10 days, and all larvae died within 6 days after inoculation. About 60% of larvae survived until 22 days after inoculation in paddy water adjusted to over pH 6.7 by adding Ca(OH)2. The brooding individuals appeared from 14 days after inoculation and ovipositing behavior was frequently observed. It was determined that the boundary of suitable and unsuitable water pH for larval survival was between 5.7 and 5.9, and the larvae can grow to the ovipositional stage by rectification of soil acidity.

Yolk protein synthesis in the riceland tadpole shrimp,Triops longicaudatus, measured by in vitro incorporation of3H-leucine

Investigation of reproductive control within the tadpole shrimp, Triops longicaudatus, required the isolation and characterization of the yolk protein (vitellin, Vn). To this end, tadpole shrimp were cultured in environmental chambers (29 degrees C-22 degrees C, with 14:10 light:dark cycle). Desiccated cysts hatched in 2-3 days after inundation. The tadpole shrimp began egg deposition 7 to 8 days after hatching and exhibited a mean growth rate of 1.85 +/- 0.24 mm/day. It was observed that 4-day-old shrimp had visible eggs in their ovaries. In addition, Vn was isolated and characterized from reproductive animals, resolving as one protein on native PAGE, and possessing a molecular weight (MW) of 376,000 +/- 2,900 as determined by FPLC. Examination by SDS-PAGE revealed that Vn is composed of a single molecule with a MW of 214,000 +/- 2,000. Methyl farnesoate (MF), a crustacean compound whose role in reproduction is still being elucidated and is structurally similar to juvenile hormone III (JH III) was incubated with ovarian explants. These explants were incubated for 24 h at room temperature in EAGLE's medium adjusted to Van Harreveld's solution in six concentrations (1 pM to 100 nM) of MF and JH III. Methyl farnesoate and JH III had no direct in vitro effect on yolk protein synthesis (P < or = 0.545 and P < or = 0.815, respectively).

Yolk protein synthesis in the riceland tadpole shrimp, Triops longicaudatus, measured by in vitro incorporation of 3H‐leucine

Yolk protein synthesis in the riceland tadpole shrimp, Triops longicaudatus, measured by in vitro incorporation of 3H‐leucine

Branchiopod Phylogenetic Reconstruction from 12s rDNA Sequence Data

ABSTRACT Nucleotide sequences from mitochondrial 12S ribosomal DNA are determined for 7 species of branchiopod crustaceans: 2 from the order Anostraca (Streptocephalus texanus and Linderiella santarosae), 2 from the order Conchostraca (Cyzicus mexicanus and Eulimnadia texana), 2 from the order Notostraca (Triops longicaudatus and Lepidurus bilobatus), and one from the order Cladocera (Moina brachycephala). They are compared to other branchiopod (Anostraca: Artemia franciscana, Cladocera: Daphnia pulex), and maxillopod (Branchiura: Savignium crenatum)sequences from the literature. The total set of nucleotides analyzed consists of sequences ranging in length from 250-267 bases. Multiple sequence alignments are generated and compared to assess the effects of alignment ambiguity on phylogenetic inference. Comparison of sequences among taxa revealed that (1) there is sufficient variation for phylogenetic analysis, (2) the variation is phylogenetically informative within and between some branchiopod orders, and (3) deep-branch phylogenetic resolution is limited by saturation effects. Phylogenetic relationships are inferred by parsimony analysis treating gaps as characters, confidence limits are estimated by both bootstrapping and the decay index. With a maxillopod sequence (Savignium crenatum) designated as an outgroup, the following results are obtained: branchiopod orders are monophyletic as sampled in this survey, with the orders Conchostraca and Notostraca clustering as sister taxa. Evidence for lineage specific rate heterogeneity of molecular evolution is discussed.

Limb development in a primitive crustacean, Triops longicaudatus : subdivision of the early limb bud gives rise to multibranched limbs

Recent advances in developmental genetics of Drosophila have uncovered some of the key molecules involved in the positioning and outgrowth of the leg primordia. Although expression patterns of these molecules have been analyzed in several arthropod species, broad comparisons of mechanisms of limb development among arthropods remain somewhat speculative since no detailed studies of limb development exist for crustaceans, the postulated sister group of insects. As a basis for such comparisons, we analysed limb development in a primitive branchiopod crustacean, Triops longicaudatus. Adults have a series of similar limbs with eight branches or lobes that project from the main shaft. Phalloidin staining of developing limbs buds shows the distal epithelial ridge of the early limb bud exhibits eight folds that extend in a dorsal ventral (D/V) arc across the body. These initial folds subsequently form the eight lobes of the adult limb. This study demonstrates that, in a primitive crustacean, branched limbs do not arise via sequential splitting. Current models of limb development based on Drosophila do not provide a mechanism for establishing eight branches along the D/V axis of a segment. Although the events that position limbs on a body segment appear to be conserved between insects and crustaceans, mechanisms of limb branching may not.

Sensitivity of Metabolic Rate, Growth, and Fecundity of Tadpole Shrimp Triops longicaudatus to Environmental Variation.

The influence of fluctuations of ambient oxygen tensions and temperature on the rate of oxygen consumption (VO2) was determined for the tadpole shrimp, Triops longicaudatus. VO2 was oxygen dependent up to 185 torr PO2, and Q10 for oxygen consumption between 20° and 30°C was 1.9. From these results it was estimated that oxygen consumption increases more than 1100 μl · g-1 · h-1 in T. longicaudatus for typical diurnal changes in temperature and oxygen in desert ephemeral pools. Elevated VO2 may be coupled with increased growth rate and fecundity, because these characteristics were highly sensitive to changes in ambient temperature and oxygen tension. Depressing mean daily temperatures by 2.3°C significantly decreased body mass, whereas hyperoxia (200 torr) significantly increased growth compared to that of animals raised under hypoxic conditions (70 torr). Fecundity was dependent on animal mass and ambient oxygen tension. Thus, for a 22-day season, one T. longicaudatus female could produce 30 more eggs per 10 torr increase in oxygen tension and 43 more eggs per 1°C change in mean daily temperature. These results indicate that there are selective pressures for metabolic sensitivity to the high temperature-high oxygen conditions of the ephemeral environments inhabited by T. longicaudatus.

高知県で発見されたアメリカカブトエビＴｒｉｏｐｓ ｌｏｎｇｉｃａｕｄａｔｕｓ，および田面水の溢水が本種の発生に及ぼす影響について

The tadpole shrimp, Triops longicaudatus, was found in several rice paddies in Kochi Prefecture. Annual fluctuation in its occurrence is due to loss of floating eggs by occasional overflow of paddy water.