Marine incursions,cryptic species and ecological diversification in Amazonia: the biogeographic history of the croaker genus Plagioscion (Sciaenidae)

Aim We propose a phylogenetic hypothesis for the marine‐derived sciaenid genus Plagioscion in the context of geomorphology and adaptation to freshwaters of South America, and assess the extent to which contemporary freshwater hydrochemical gradients influence diversification within a widely distributed Plagioscion species, Plagioscion squamosissimus. Location Amazon Basin and South America. Methods Using nuclear and mitochondrial DNA sequence data, phylogenetic analyses were conducted on the five nominal Plagioscion species, together with representatives from Pachyurus and Pachypops, using character and model‐based methods. Genealogical relationships and population genetic structure of 152 P. squamosissimus specimens sampled from the five major rivers and three hydrochemical settings/‘colours’ (i.e. white, black and clear water) of the Amazon Basin were assessed. Results Phylogenetic analyses support the monophyly of Plagioscion in South America and identify two putative cryptic species of Plagioscion. Divergence estimates suggest that the Plagioscion ancestor invaded South America via a northern route during the late Oligocene to early Miocene. Within P. squamosissimus a strong association of haplotype and water colour was observed, together with significant population structure detected between water colours. Main conclusions Our analyses of Plagioscion are consistent with a biogeographic scenario of early Miocene marine incursions into South America. Based on our phylogenetic results, the fossil record, geomorphological history and distributional data of extant Plagioscion species, we propose that marine incursions into western Venezuela between the late Oligocene and early Miocene were responsible for the adaptation to freshwaters in Plagioscion species. Following the termination of the marine incursions during the late Miocene and the establishment of the modern Amazon River, Plagioscion experienced a rapid diversification. Plagioscion squamosissimus arose during that time. The formation of the Amazon River probably facilitated population and range expansions for this species. Further, the large‐scale hydrochemical gradients within the Amazon Basin appear to be acting as ecological barriers maintaining population discontinuities in P. squamosissimus even in the face of gene flow. Our results highlight the importance of divergent natural selection through time in the generation and maintenance of sciaenid diversity in Amazonia.     

Genetic relationships of Plagioscion squamosissimus (Perciformes,Sciaenidae) from five Neotropical river basins evaluated using mitochondrial atpase6/8 gene sequences

The genetic relationships of native or introduced Plagioscion squamosissimus in five Brazilian Neotropical basins were evaluated using the mitochondrial atpase6/8 genes. Results revealed that the population of the Tocantins River basin is more basal than the native populations of the Amazon and Parnaíba River basins. Moreover, the populations of P. squamosissimus that were introduced in the São Francisco and upper Paraná River basins originated from the population of the Parnaíba River.     

Morphology and molecular phylogeny of Pauciconfibuloides amazonica gen. n. sp. n. (Platyhelminthes,Monogenoidea) parasitizing the Amazonian croaker Plagioscion squamosissimus

An integrative study was performed to understand the phylogenetic relationships of an undescribed, freshwater species of microcotylid parasitizing Plagioscion squamosissimus from the Amazon River Basin. Based on morphological and molecular analysis (18S rDNA and partial 28S rDNA genes), a new genus is proposed to accommodate this new species, Pauciconfibuloides amazonica gen. n. sp. n. The new genus is closely related to Protastomicrocotylinae and Pauciconfibula by sharing the vagina, male copulatory organ, and genital atrium all unarmed. However, Pauciconfibuloides gen. n. can be distinguished from those taxa by the prostatic system and position of the vaginal pore. Molecular phylogenetic inference suggests a sister relationship with species of Polylabris (Prostatomicrocotylinae), but to date, there are no available 18S or 28S rDNA sequences of Pauciconfibula to be compared. This is the first report of a microcotylid parasitizing a freshwater sciaenid from South America.     

Therodamas tamarae, a new species of copepod (Poecilostomatoida: Ergasilidae) parasitic on Plagioscion squamosissimus (Heckel) from the Araguaia River, Brazil; with a key to the species of the genus

Therodamas tamarae n.sp. is described based on females removed from branchial filaments of Plagioscion squamosissimus (Teleostei, Sciaenidae) caught in a lake near the Araguaia River, State of Goiás, Brazil. The new species shares with Therodamas elongatus (Thatcher, 1986) the same host, a similar reaction from the host to the presence of the parasites, and the same general shape of body; in addition, the two species are from the Amazon basin. On the other hand, it resembles T. fluviatilis Paggi, 1976 in the structure of legs 1 to 4. An identification key for Therodamas species, as well as comments on the distribution of the species, are included.     

The reproductive biology of Plagioscion squamosissimus (Heckel, 1840) in the Pará River estuary (Amazon Estuary)

This study describes the reproductive biology of the South American silver croaker Plagioscion squamosissimus (Heckel, 1840) in the Pará River estuary. Data were collected bimonthly from June 2007 to May 2008. In all, 334 specimens were examined. The gonads were processed with histological techniques, and the ovaries were subjected to morphometric analysis. The length at first maturity (L₅₀) values were 16.14 and 21.43 cm total length for females and males, respectively. The sex ratio based on the total number of individuals favoured the females (1.11 females: one male). Macroscopically, the gonads were classified as immature (A), maturing (B), mature (C) and spent (D). Microscopically, four germ cell types were distinguished based on the development of the ovaries. Chromatin nucleolus (I), perinucleolar (II), cortical alveoli (III) and full‐vitellogenic (IV) oocytes were observed in all ovarian stages, except that of the mature individuals which showed the largest number of full‐vitellogenic oocytes (IV), with a mean diameter of 565.4 μm (±147.4). Substantial percentages of individual P. squamosissimus were found to be in a reproductive condition. Reproductive activity was recorded throughout the year in the Pará River estuary, primarily in February/March and August/September.     

Ultrastructure of spermiogenesis in Plagioscion squamosissimus (Teleostei, Perciformes, Sciaenidae)

Spermiogenesis in Plagioscion squamosissimus occurs in cysts. It involves a gradual differentiation process of spermatids that is characterized mainly by chromatin compaction in the nucleus and formation of the flagellum, resulting in the spermatozoa, the smallest germ cells. At the end of spermiogenesis, the cysts open and release the newly formed spermatozoa into the lumen of the seminiferous tubules. The spermatozoa do not have an acrosome and are divided into head, midpiece, and tail or flagellum. The spermatozoa of P. squamosissimus are of perciform type with the flagellum parallel to the nucleus and the centrioles located outside the nuclear notch.     

The influence of seasonality,fish size and reproductive status on EROD activity in Plagioscion squamosissimus: Implications for biomonitoring of tropical/subtropical reservoirs

Ethoxyresorufin-O-deethylase (EROD) activity is considered an important biomarker for aquatic environmental contamination. Although EROD activity has been widely used as a biomarker of exposure to polycyclic aromatic hydrocarbons in fish, this activity can be influenced in the field by spatial-, seasonal- or individual-related factors. We therefore performed a comparative study of hepatic EROD activity levels in the croaker Plagioscion squamosissimus to determine whether variations existed in enzyme activity levels, especially in relationship to reproductive status, fish size, age, and seasonality. For this purpose, we collected fish from three reservoirs with different pollution levels during the early-rainy (November 2012), rainy (March 2013), and dry (July–August 2013) seasons from the Tietê River, Brazil. We tested whether size, age and sex affected EROD activity among the localities and seasons. We found a marked effect of pollution during the dry season on variation among the localities in EROD activity in P. squamosissimus. An analysis of covariance indicated that sex had a significant negative effect on the seasonal variability of the EROD activity levels at the most polluted locality (near São Paulo). A possible explanation for the statistical association between EROD activity and sex is that the reproductive status of the females influenced the EROD activity levels. A possible explanation for the statistical association between EROD activity and sex is that the reproductive status of the females influenced the EROD activity levels, also largely reported in the literature. Our results suggest that reproductive status can be a significant confounding factor for determining EROD activity in female P. squamosissimus in freshwater ecosystems when compared to males. Moreover, our results suggest that the presence of phenanthrene during the dry season at Barra Bonita reservoir might explain the highest EROD activity responses in this period of study.     

Transferrin polymorphism in Central Amazon populations of pescada, Plagioscion squamosissimus

Blood plasma of 253 specimens from eight population samples of the sciaenid fish, pescada (Plagioscion squamosissimus), caught from four sites in the Central Amazon, was tested for molecular variants of transferrin. Starch gel electrophoresis was used to distinguish six species of transferrin molecules; 12 of the 21 theoretically possible genotypes were found. There were highly significant departures from genetic equilibrium in seven of the eight population samples (chi-square (chi(2)) test for Hardy-Weinberg expectations) due to an excess of homozygotes and a corresponding deficiency of heterozygotes. A dendrogram based on UPGMA cluster analysis of genetic distances at the transferrin gene locus, estimated among the population samples and statistical analyses of the distribution of Tf allele frequencies, indicated three genetically discreet sub-populations of P. squamosissimus. The three sub-populations, "Careiro/Iranduba", "Coari" and "Tefe", were found to have high frequencies of alleles Tf(2), Tf(4) and Tf(3), respectively. This genetic instability may be attributed to genetically discreet "allopatric stocklets", which diverged during past isolation.     

Length‐weight relationship of 11 fish species from a tributary of the Amazon River system in northern Brazil

The length–weight relationships (LWRs) of 11 freshwater fish for eight families (Leporinus friderici, Pterophyllum scalare, Geophagus camopiensis, Curimata incompta, Astyanax bimaculatus, Tetragonopterus chalceus, Moenkhausia lepidura, Metynnis lippincottianus, Plagioscion squamosissimus, Hemiodus unimaculatus and Colomesus asellus) captured in tributary of the Amazon River system (Brazil) were investigated. These results represent the first reference on the LWRs for all 11 species in the eastern Amazon.     

Larval fish assemblage in the Baía River (Mato Grosso do Sul State,Brazil): temporal and spatial patterns

Synopsis We sampled the Baía River (Mato Grosso do Sul State, Brazil) monthly, to survey taxonomic composition and temporal and spatial distribution of fish larvae. The ichthyoplankton was mainly composed by larvae of small and medium sized sedentary species and it was numerically dominated by six taxa: Plagioscion squamosissimus, Hypophthalmus edentatus, Hoplias aff. malabaricus, Bryconamericus stramineus, Serrasalmus spp. and Catathyridium jenynsii. These taxa present distinct temporal and spatial occurrence patterns: H. edentatus, B. stramineus and C. jenynsii are abundant between September and March in lentic areas; H. aff. malabaricus and Serrasalmus spp. were caught between October and February in lotic areas; whereas P. squamosissimus occurs in all sampled areas, with peak of capture in January. Hypophthalmus edentatus, H. aff. malabaricus, Serrasalmus spp. and B. stramineus were the taxa that most contributed to structure the assemblages temporally and spatially, and their abundances were influenced by the interaction of several environmental variables.     

Influence of flood pulses on diet composition and trophic relationships among piscivorous fish in the upper Paraná River floodplain

The aim of this article is to evaluate whether alterations in flood pulses differentially affect diet composition, feeding niche breadth, and diet overlap of piscivorous fish. Species examined were Acestrorhynchus lacustris, Hoplias aff malabaricus, Plagioscion squamosissimus, Rhaphiodon vulpinus, and Salminus brasiliensis. These species were collected with gillnets (different mesh sizes) in the upper Paraná River floodplain, during four distinct flood events (four periods; A = 1992/1993; B = 2000; C = 2001; and D = 2002). The volumetric method was chosen to express diet results. Feeding niche breadth was calculated using Levins measure, and diet overlap was evaluated by the Pianka’s Index. Flooding was more intense and lasted longer in the first period (1992/1993—A). Diet composition of the studied species was broad (47 total items consumed). For period A, Prochilodus lineatus was the main item taken by four out of five species. In the other periods, there were relevant alterations in diet, since P. lineatus was not recorded in any stomach of the five species; rather, it was replaced by the shrimp, Macrobrachium amazonicum. Diet overlap was low in all periods. The greatest overlap was obtained in period C for P. squamosissimus and R. vulpinus, due to high consumption of shrimps. There were no significant differences in niche breadth among species. However, the species presented distinct variation patterns in niche breadth. For example, H. aff. malabaricus showed a tendency toward increasing niche over the period, but the other species presented larger niches only during period A. Therefore, it can be concluded that the intensity and duration of the flood pulse influences: (i) the diet composition of piscivores; (ii) the breadth of their niches; and (iii) feeding overlap among species. Handling editor: J. Cambray     

Fish Communities in Central Amazonian White- and Blackwater Floodplains

In Amazonian floodplains, the flood cycle of the river is becoming the dominant seasonal factor, and fish communities are found to fluctuate greatly over the year. During inundation, fish migrate into floodplain forests to feed on fruits and seeds, in an area more than 300000km² in size. To document patterns of species diversity, distribution, abundance and temporal dynamics and in order to describe the ecological importance of the inundated forest, floodplain fish were captured using variously sized gill nets in white and black water areas inside and outside the floodplain forests during low, rising, high and falling water level in 1990 and 1991. Dominance varies to some extent in white water between floodplain forest (0.06) and open water (0.11) while it is unchanged in black water (0.04). Black water fish communities were more diverse. Most abundant among white water fish were Liposarcus pardalis, Pygocentrus nattereri, and Pellona flavipinnis, for example, or Plagioscion squamsissimus, Serrasalmus rhombeus, and Serrasalmus manueli in black water. Among the most abundant white water fish, Colossoma macropomum, Mylossoma duriventre and Osteoglossum bicirrhosum occurred almost exclusively in inundated forests. Of the black water species there were a large number of species which were captured only in inundated forest, such as Geophagus cf. altifrons, Hoplias malabaricus, Osteoglossum bicirrhosum and Uaru amphiacanthoides. Catches varied with sample site, water level and direction of water level change. The average CPUE in white and black water was 190 and 41g fishm^–2 and day, respectively, with maximum yields at low water and minimum yields at high water. Comparing rising and falling water levels, a significantly higher quantity of fishes was captured at falling water level. In black water, fish catches from the floodplain forest exceeded the open water catch by 183 to 550%, depending on season. Differences in respect of white water are smaller (106–281%). Fish communities in the area under investigation seem to be stochastically assembled, with significant differences between white and black water only. Many fishes move into the floodplain forest not only to feed but probably also for other reasons – to seek shelter, for example.     

Effect of flood pulses on the trophic ecology of four piscivorous fishes from the eastern Amazon

This study investigated the effect of hydrological periods on the feeding activity and trophic interactions of four piscivorous fishes from the middle Xingu River, Brazil: pike‐characid Boulengerella cuvieri, dogtooth characin Hydrolycus armatus, dogtooth characin Hydrolycus tatauaia and South American silver croaker Plagioscion squamosissimus. Repletion Index (I_R%), Alimentary Index (I_Ai%) and food web properties were calculated for each species. A total of 825 specimens were collected. The I_R showed changes in feeding intensity of B. cuvieri, H. armatus and H. tatauaia among hydrological periods. Flood pulse showed no influence on composition and importance of food items consumed. Trophic connections showed that connectivity ranged from 0.025 to 0.038. The highest number of trophic connections (75) occurred in the high‐water period, when 51 food items were recorded and the lowest number of trophic connections (43) occurred in receding water, with 31 food items. In all food webs, over 45% of food items were consumed by only one species (ultra‐peripheral items), which is common in piscivorous fishes.     

Spatiotemporal Variability and Sound Characterization in Silver Croaker Plagioscion squamosissimus (Sciaenidae) in the Central Amazon

Background

The fish family Sciaenidae has numerous species that produce sounds with superfast muscles that vibrate the swimbladder. These muscles form post embryonically and undergo seasonal hypertrophy-atrophy cycles. The family has been the focus of numerous passive acoustic studies to localize spatial and temporal occurrence of spawning aggregations. Fishes produce disturbance calls when hand-held, and males form aggregations in late afternoon and produce advertisement calls to attract females for mating. Previous studies on five continents have been confined to temperate species. Here we examine the calls of the silver croaker Plagioscion squamosissimus, a freshwater equatorial species, which experiences constant photoperiod, minimal temperature variation but seasonal changes in water depth and color, pH and conductivity.

Methods and Principal Findings

Dissections indicate that sonic muscles are present exclusively in males and that muscles are thicker and redder during the mating season. Disturbance calls were recorded in hand-held fish during the low-water mating season and high-water period outside of the mating season. Advertisement calls were recorded from wild fish that formed aggregations in both periods but only during the mating season from fish in large cages. Disturbance calls consist of a series of short individual pulses in mature males. Advertisement calls start with single and paired pulses followed by greater amplitude multi-pulse bursts with higher peak frequencies than in disturbance calls. Advertisement-like calls also occur in aggregations during the off season, but bursts are shorter with fewer pulses.

Conclusions and Significance

Silver croaker produce complex advertisement calls that vary in amplitude, number of cycles per burst and burst duration of their calls. Unlike temperate sciaenids, which only call during the spawning season, silver croaker produce advertisement calls in both seasons. Sonic muscles are thinner, and bursts are shorter than at the spawning peak, but males still produce complex calls outside of the mating season.     

Warning coloration in sawflyAthalia rosae larva and concealing coloration in butterflyPieris rapae larva feeding on similar plants evolved through individual selection

Green larvae of the butterfly Pieris rapae and black larvae of the sawfly Athalia rosae feed on green leaves of the same cruciferous plants. To demonstrate that P. rapae has concealing coloration and that A. rosae has warning coloration, the larvae of the two species were supplied to naive chicks Gallus gallus on white, green or black backgrounds. P. rapae larvae were palatable and their green body color acted as a concealing coloration. On the other hand, A. rosae larvae were unpalatable and their black body color acted as a warning coloration. There is a general consensus that warning coloration is an altruistic character which needs victims, and thus can evolve through kin selection or green beard selection. However, black A. rosae larvae were seldom injured by chicks' attack, in particular, on the green background. Therefore, the warning coloration of A. rosae larvae can be a selfish character and hence can evolve through individual selection as well as concealing coloration of P. rapae.     

Testing Wallace's intuition: water type,reproductive isolation and divergence in an Amazonian fish

Alfred Russel Wallace proposed classifying Amazon rivers based on their colour and clarity: white, black and clear water. Wallace also proposed that black waters could mediate diversification and yield distinct fish species. Here, we bring evidence of speciation mediated by water type in the sailfin tetra (Crenuchus spilurus), a fish whose range encompasses rivers of very distinct hydrochemical conditions. Distribution of the two main lineages concords with Wallace's water types: one restricted to the acidic and nutrient‐poor waters of the Negro River (herein Rio Negro lineage) and a second widespread throughout the remaining of the species’ distribution (herein Amazonas lineage). These lineages occur over a very broad geographical range, suggesting that despite occurring in regions separated by thousands of kilometres, individuals of the distinct lineages fail to occupy each other's habitats, hundreds of metres apart and not separated by physical barrier. Reproductive isolation was assessed in isolated pairs exposed to black‐water conditions. All pairs with at least one individual of the lineage not native to black waters showed significantly lower spawning success, suggesting that the water type affected the fitness and contributed to reproductive isolation. Our results endorse Wallace's intuition and highlight the importance of ecological factors in shaping diversity of the Amazon fish fauna.     

Pennahia ovata,a new sciaenid from the Bay of Bengal

A new sciaenid,Pennahia ovata, is described from the Bay of Bengal. It differs from its most similar congener,P. anea, in having weakly differentiated teeth on the lower jaw, usually 24–25 dorsal fin soft rays and 18–19 upper+lower gill rakers, a deep body and a long second anal fin spine.     

Functional morphology of gills and respiratory area of two active rheophilic fish species, Plagioscion squamosissimus and Prochilodus scrofa

Measurements of gill dimensions were carried out on two ecologically distinct active rheophilic teleost species, the curvina Plagioscion squamosissimus and the curimbatá Prochilodus scrofa , and were analysed in relation to body mass according to the equation Y=aW^b . The gill respiratory areas of P. squamosissimus and P. scrofa were large as expected for active fish and increased with increasing body mass ( b =0.70 and 0.72, respectively) showing no significant difference between them. However, the large respiratory area of both species was realized in a different way revealing an adaptation to the plasticity of head components related to feeding habits. Consequently, significant differences were found between the number and average length of gill filaments and the bilateral area of secondary lamellae. The respiratory area of P. scrofa was due mainly to larger bilateral surface area of the secondary lamellae and its growth coefficient ( b =0.51) that was significantly higher ( P <0.05) than that found for P. squamosissimus ( b = 0.36). The frequency of secondary lamellae mm⁻¹ of filament was similar in both species (22 ± 2 on one side of gill filament). The dimensions of gill components and the respiratory area of these species suggest a complex interaction between head form, and feeding habits related to the functional morphology of the gills to meet the oxygen requirements of each species.     

Aedes albopictus oviposits with other Aedes species in artificial oviposition cups: a case study in Knox County,Tennessee, U.S.A.

Interspecific associations between two mosquito species can lead to effects such as competition, species displacement, and species stability. To better understand Aedes albopictus (Skuse) and other Aedes species, we monitored eggs in artificial oviposition cups (ovitraps) within Knox County, TN, U.S.A., during the 2016 and 2017 mosquito seasons. In 2016, one black and one white ovitrap were placed at 18 sites for 21 weeks, while in 2017 black and white ovitraps baited with grass‐infused or deionized water were placed at 11 sites for nine weeks. Eggs were identified to species and resulting counts were used to determine the degree of interspecific association using Cole's coefficients (C₇) and the degree of heterogeneity across space and time using generalized linear mixed models (GLMM). Here, Aedes mosquitoes are generally ovipositing in black cups with grass‐infused water, and Ae. albopictus eggs co‐occurred with other Aedes species more often than would be expected. Finding a positive significant interspecific association between Ae. albopictus and other Aedes eggs suggests that methods used to control Ae. albopictus may also control other Aedes mosquitoes. Finding that Ae. albopictus co‐occurs with other Aedes mosquitoes warrants additional research to evaluate outcomes associated with co‐occurrence within the study area.     

Race Differences in Accuracy of Self‐Reported Childhood Body Size Among White and Black Women

Objective: To assess the relation of self‐reported current and recalled preadolescent body size to measured BMI (kilograms per meter squared) and interviewer's assessment of body size. Research Methods and Procedures: This was a prospective cohort study of 1890 white and black women who were 9 to 10 years old at time of enrollment and were followed up 10 to 13 years later. At baseline, subjects had their weight and height measured and were asked to indicate their current body size from a series of nine pictograms. A sample of the subjects also had their body size evaluated by interviewers. At the young‐adult follow‐up visit, subjects were asked to recall their body size at 9 and 10 years old and to indicate their current weight, height, body size, and level of concern with weight. Results: Among the women with interviewer assessments, 84% of the white women and 67% of black women recalled a body size that was within one body size of the interviewer's assessment. Independent of weight status in childhood or at follow‐up, black women were 3 times more likely than white women to recall a body figure that was more than one figure leaner than the shape they reported at baseline (odds ratio = 3.5, 95% confidence interval 2.8 to 4.5) or than the interviewer's rating at baseline (odds ratio = 3.4, 95% confidence interval 2.4 to 4.9). Discussion: The results suggest that the use of body figures to recall childhood size are best suited for ranking subjects in terms of BMI. The higher rate of underestimation of size by black women suggests that body figure ratings work best for white women.