Growth and longevity of the protogynous parrotfish,Hipposcarus harid,Scarus ferrugineus and Chlorurus sordidus (Teleostei,Scaridae), off the eastern coast of the Red Sea

Growth and longevity were studied for three species of the family scaridae, the longnose parrotfish (Hipposcarus harid), rusty parrotfish (Scarus ferrugineus) and bullethead parrotfish (Chlorurus sordidus), sampled at the eastern coast of the Red Sea, off Saudi Arabia. The three species are protogynous hermaphrodites presenting two distinct phases whereby the initial phase includes females and primary males, and the terminal phase is exclusively secondary males transformed from females. Annual marks in the ctenoid scales from the three species were used to develop size‐at‐age plots. Linear relationships were found between the scale radius and standard length for the three species, and the relationships between body weight (w) and standard length (L) were estimated. Scales of these species increased in size consistently throughout life, even though the somatic growth rate decreased with age. Sex‐specific growth effects in the three species were demonstrated. Growth of initial phase females was the lowest, followed by the initial phase males and terminal phase males, the latter showing the fastest growth rates. Thus, transition to the terminal male identity was associated with enhanced growth, resulting in larger terminal males than females of equivalent size. The von Bertalanffy growth formula (VBGF) was estimated for H. harid, S. ferrugineus and C. sordidus (L_∞ = 43.92, 27.4 and 23.3; K = 0.067, 0.27 and 0.56; t₀ = ?6.92, ?4.98 and ?4.6, respectively). The relationship between growth and reproduction of these species is also discussed.     

Chronic spearfishing may indirectly affect reef health through reductions in parrotfish bite rates

The grazing behaviour of two Caribbean parrotfish, a fished species, the stoplight parrotfish Sparisoma viride and a non-fished species, the striped parrotfish Scarus iseri, were studied in the presence (fished site) and absence (marine reserve) of chronic spearfishing activity. Diurnal feeding periodicity did not differ between the sites in either species: roving individuals had significantly higher bite rates in the afternoon, while territorial individuals foraged consistently throughout the day. Mean bite rate varied between sites in both species. Abundance, biomass and bite rates of S. viride were all significantly higher within the reserve, except for roving S. viride which had a higher mean bite rate in the afternoon outside the reserve compared with within it, attributable to maximisation of feeding in the afternoon when fishing risk was lower. Scarus iseri mean abundance and bite rate were greater outside the reserve, potentially because reduction in large territorial herbivores allowed S. iseri to feed more rapidly. By reducing the grazing potential of the remaining S. viride individuals the effect of fishing is greater than would be predicted from biomass changes alone. Less grazing by S. viride would not be compensated for by the increase in grazing by S. iseri because the latter feeds on different algae. Spearfishing of key parrotfish species reduces grazing potential directly by extraction and indirectly by changing behaviour.     

The non-linear relationship between body size and function in parrotfishes

Parrotfishes are a group of herbivores that play an important functional role in structuring benthic communities on coral reefs. Increasingly, these fish are being targeted by fishermen, and resultant declines in biomass and abundance may have severe consequences for the dynamics and regeneration of coral reefs. However, the impact of overfishing extends beyond declining fish stocks. It can also lead to demographic changes within species populations where mean body size is reduced. The effect of reduced mean body size on population dynamics is well described in literature but virtually no information exists on how this may influence important ecological functions. The study investigated how one important function, scraping (i.e., the capacity to remove algae and open up bare substratum for coral larval settlement), by three common species of parrotfishes (Scarus niger, Chlorurus sordidus, and Chlorurus strongylocephalus) on coral reefs at Zanzibar (Tanzania) was influenced by the size of individual fishes. There was a non-linear relationship between body size and scraping function for all species examined, and impact through scraping was also found to increase markedly when fish reached a size of 15–20 cm. Thus, coral reefs which have a high abundance and biomass of parrotfish may nonetheless be functionally impaired if dominated by small-sized individuals. Reductions in mean body size within parrotfish populations could, therefore, have functional impacts on coral reefs that previously have been overlooked.     

Lack of a genetic bottleneck in a recent Lessepsian bioinvader, the blue-barred parrotfish, Scarus ghobban

The present study investigates the genetic diversity of Scarus ghobban, a recently introduced parrotfish in the Mediterranean Sea via the Suez Canal. Two mitochondrial and one nuclear DNA regions were sequenced and phylogenetic relationships investigated, from samples collected from Lebanon and across its natural range. Scarus ghobban clustered in two major clades, Pacific Ocean and Indian Ocean, indicating strong population structure, or cryptic speciation. Expectedly, Mediterranean samples clustered with Indian Ocean-Red Sea individuals. However, unlike other recent Lessepsian invaders, S. ghobban displayed high genetic diversity. These results underscore that genetic diversity is a poor predictor of success of an invasive species.     

Seaweed survival after consumption by the greenbeak parrotfish,Scarus trispinosus

We assessed the survival of seaweed (macroalgae and cyanobacteria) after consumption by the greenbeak parrotfish, Scarus trispinosus, in northeastern Brazil. Samples of S. trispinosus feces were collected, inoculated on filter paper, and kept in the laboratory and field for 60 and 30 d, respectively. Comparisons of samples inoculated with feces to those without (controls) revealed a marked increase in the abundance and diversity of seaweed in samples inoculated with feces in both laboratory and field experiments. These results were consistent between summer and winter, although the seaweed species differed. A total of one cyanobacterium and 16 macroalgal taxa (nine rhodophytes, five heterokontophytes, and two chlorophytes) were recorded in the inoculated samples. Rhodophyta also presented the highest abundance across treatments, possibly because of their higher resistance to parrotfish digestion, greater ingestion, or both. The survival of cyanobacteria and macroalgae after consumption by S. trispinosus suggests that parrotfishes may contribute to seaweed dispersion on tropical reefs.

     

Growth and maturation of the redlip parrotfish Scarus rubroviolaceus

This study presents age‐based life‐history information for the red lip parrotfish Scarus rubroviolaceus based on a 5 year sampling programme from the commercial fishery of American Samoa. Females reached sexual maturity at 31·9 cm fork length (L_F) and 2·6 years and sex change occurred at 42·3 cm L_F, although not all females change sex through their ontogeny. The maximum observed age was 14 years and c. 65% of the fishery harvest was above the median L_F at sex change.     

Alternative male mating tactics of the endemic Red Sea parrotfish Scarus ferrugineus

The present study shows that small non‐territorial terminal‐phase males of the rusty parrotfish Scarus ferrugineus are reproductively active and are comparable with initial‐phase males in behaviour, rates of participation during group‐spawning and success in streaking into pair spawning. Large territorial terminal‐phase males defend contiguous territories for several hours during the morning where they pair spawn with initial‐phase females.     

Comparisons of body sizes at sexual maturity and at sex change in the parrotfishes of Hawaii: input needed for management regulations and stock assessments

First estimates of sex allocation patterns and body size‐at‐sexual maturity and at protogynous sex change are presented for the five major (including one endemic) species of parrotfishes of Hawaii. Median body size at initial maturation as a female (L_M50) and at protogynous sex change from adult female to adult male (L_Δ50) varied greatly among the five species. Estimates of L_M50 were about 14, 17, 24, 34 and 35 cm fork length (L_F) in palenose Scarus psittacus, Pacific bullethead Chlorurus spilurus, stareye Calotomus carolinus, spectacled Chlorurus perspicillatus and redlip parrotfish Scarus rubroviolaceus. Values of L_Δ50 were c. 23, 27, 37, 46 and 47 cm L_F in the respective species. Length at female maturation was proportional to maximum body size (L_max) of the respective species, ranging from 50 to 72% and averaging 62% of L_max across species. L_Δ50 was also proportional to L_max, ranging from 82 to 97% and averaging 92%. Males of both pairs of Scarus and Chlorurus spp. reported here are diandric. Only one of the five major species (C. carolinus) is functionally monandric, with either all or nearly all males secondarily derived from adult females. The broadly differing absolute body sizes at sexual maturation and at sex change among the five species have important implications for improving regulatory size limits for parrotfishes in the State of Hawaii, where parrotfish species have historically been managed based on a single minimum size limit of 30·5 cm L_F. This study provides a model demonstration of why catch data for parrotfishes, and other size‐structured reef‐fish populations, should be recorded either by species or by functional size‐groups of species that allow setting more meaningful minimum size limits.     

Scarus obishime,a new parrotfish (Perciformes: Scaridae) from the Ogasawara Islands

Scarus obishime is described as a new species of parrotfish from the Ogasawara Islands from five specimens. It is characterized as follows: 6–7 median predorsal scales, a single scale in third row on cheek, 15 pectoral rays, terminal male with a prominent bulging snout and forehead; initial-phase fish yellowish brown with an irregular white lateral stripe posteriorly on body; terminal male deep blue with a broad yellow bar on body.     

Length–weight relationships of six coral reef‐fish species from Chuuk,Federated States of Micronesia

Length–weight relationships (LWR) were estimated for six reef species in Chuuk lagoon (Federated States of Micronesia) captured by commercial fishers. Specimens were sampled opportunistically over a period of 2 months between July and September 2014. Relationships include those for four common species not currently reported in FishBase (Caesio teres, Myripristis adusta, Lethrinus erythracanthus, and Chlorurus frontalis), and for two species with relationships based on just one or two samples (Scarus oviceps, and Plectropomus oligacanthus). While estimates for some species are tentative given limited size‐range sampling, they still present an improvement in the currently available LWRs.     

Two new parrotfishes of the genus Scarus from the Central and South Pacific, with further examples of sexual dichromatism

Scarus lauia (Jordan & Evermann) and Scarus formosus Valenciennes are junior synonyms oi Scarus dubius Bennett, the former based on the terminal phase and the latter on the initial phase. Scarus dubius is endemic to the Hawaiian Islands, one of five species of the genus in these islands. The initial phase of Scarus fiavipectoralis Schultz is grey to brown with whitish streaks on the abdomen, a dark caudal fin and yellow at the pectoral base. The range of this species is extended from the Philippines to the Marshall, Solomon, and Caroline Islands and the Great Barrier Reef. Scarusfasciatus Valenciennes is a junior svnonym of of the western Pacific 5. rivulatus Valenciennes. The initial phase is grey to brown with three pale stripes on the abdomen. Scarus lepidus Jenyns is a junior synonym of the wide-ranging Indo-Pacific S. globiceps Valenciennes. The initial phase is coloured like that of S. rivulatus. Scarus janthochir Bleeker, S. chlorodon Jenyns, and S. singaporensis Bleeker are junior synonyms of 5. prasiognathos Valenciennes; it occurs from the western Pacific to the Maldive Islands. Scarus elerae Jordan & Seale and S. urbanus (Smith) are junior synonyms of the wide-ranging Indo-Pacific S. tricolor Bleeker based on the terminal phase. Scarus dimidiatus Bleeker occurs in the western Pacific east to Samoa. Its initial phase, very similar to that of the western Indian Ocean S. scaber, is yellowish, shading to whitish ventrally, with five slightly diagonal dark bars on the upper half of the body. Callyodon mutabilis Gray is a junior synonym of S. quoyi Valenciennes. Scarus spinus (Kner) is the valid name for the distinctive bullet-headed parrotfish with a greenish yellow snout which was misidentified as S.formosus by Schultz. The initial phase is dark brown with pale bars. The terminal phase of the Pacific parrotfish Scarus schlegeli Bleeker is distinctive in possessing a pale bar on the side (yellow dorsally, light green ventrally). The drab initial phase with alternating dark and light bars was misidentified as S. venosus Valenciennes by Schultz, a junior synonym of S. psittacus Forsskǎl. The terminal phase of the western Pacific Scarus bleekeri de Beaufort has a characteristic large whitish patch bordered with blue-green on the cheek. The initial phase is dark brown, the edges of the scales narrowly orangish, shading to orange-red ventrally, with faint yellowish bars, caudal peduncle and caudal fin. A closely related species from Indonesia and the Andaman Sea is tentatively identified as 5. troschelii Bleeker. The terminal phase has a band of blue-green curving from the corner of the mouth to below the eye and back down to the pectoral base. Scarus japanensis (Bloch), identified in most recent papers as S. capistratoides Bleeker, is the terminal phase and senior synonym of the dark brown, red-tailed S. pyrrhurus (Jordan & Seale); it is restricted to the western Pacific (easternmost record, Samoa). Scarus gibbus Ruppell is differentiated into three populations based on colour. Scarus koputea sp. nov., unique in having four rows of scales on the cheek, is described from the Marquesas Islands. Scarus longipinnis sp. nov. is described from Pitcairn, Rapa, and the Capricorn Group of the Great Barrier Reef; its pelvic lins are longer and the dorsal fin more elevated than other Scarus.     

Territorial behaviour of <Emphasis Type="Italic">Acanthurus sohal</Emphasis> and <Emphasis Type="Italic">Plectroglyphidodon leucozona</Emphasis> on the fringing Egyptian Red Sea reefs

Synopsis We studied territorial behaviour of the acanthurid surgeonfish Acanthurus sohal and pomacentrid damselfish Plectroglyphidodon leucozona on fringing reefs in Ras Mohammed National Park, Red Sea, Egypt. We investigated trespass times, the number of agonistic acts, their intensity and the agonism elicited (number agonistic acts/total trespass time) for all intruders. Five families (Pomacentridae, Chaetodontidae, Acanthuridae, Labridae and Scaridae) were dominant among the 14 we recorded in our study sites. Seven species belonging to four families were resident inside A. sohal territories. Of the other 66 species we observed, 45 are intruders. The territory-holder did not react equally agonistically toward all these intruders. A. sohal showed a high number of agonistic acts against conspecifics and the parrotfish Cetoscarus bicolor. The intensity of the agonistic encounters, however, showed a different picture, with a low level for conspecifics and C. bicolor, respectively. A. sohal showed a high degree of agonistic intensity toward only one parrotfish, Chlorurus sordidus. The highest values of Agonism elicited were recorded against Scarus ghobban, followed by Siganus rivulatus and Zebrasoma desjardinii . Despite these high values, the intensity was relatively weak. The territories of A. sohal were large (average 12.5m²); those of P.leucozona were ca. 20 times smaller (average 0.6m²). A. sohal spent most of their time swimming (patrolling) along the territory border, stopping briefly to feed on algae. On the other hand, P. leucozona spent most of their time swimming and sheltering.     

Spatial and temporal variation in coral predation by parrotfishes on the GBR: evidence from an inshore reef

There have been few studies of coral predation by fishes on the Great Barrier Reef (GBR). However, these studies have indicated that it is an important factor that may shape coral demographics. Here, for the first time, we document the spatial and temporal variation in coral predation by parrotfishes on an inshore reef on the GBR. The densities of parrotfish feeding scars on massive Porites spp. were compared within core and non-core areas of three Chlorurus microrhinos home ranges. The density of parrotfish feeding scars on massive Porites is among the highest recorded on the GBR and elsewhere with a higher abundance of excavating feeding scars within core areas, reflecting the higher occupancy of these areas by C. microrhinos. Furthermore, excavating scars were more abundant in October than in April. This may be related to the higher nutritional quality of coral colonies in October, as coral spawning usually occurs in November at this study location. No spatial or temporal variation was noted in the abundance of feeding scars from scraping parrotfishes. The lack of temporal differences may be a result of the shallow scraping scars which would not be able to reach the gonads within coral polyps. The frequency of parrotfish predation on Porites and the spatial and temporal variation recorded herein highlight the potential importance of parrotfish corallivory on the GBR.     

Interspecific variation in spawning time and male mating tactics of the parrotfishes on a fringing coral reef at Iriomote Island,Okinawa

Spawning time and male mating tactics of parrotfishes (family Scaridae) were investigated on a fringing coral reef at Iriomote Island, Okinawa. Spawning was observed in 14 species, and more frequently in more abundant species such as Chlorurus sordidus, Scarus rivulatus and Chlorurus bowersi. At the reef-edge spawning site, C. bowersi spawned at high tide, C. sordidus spawned both at high tide and in the early morning, whereas Calotomus carolinus and most of the Scarus species such as S. rivulatus spawned only in the early morning, mostly 0630–0830 h. Spawning only in the early morning irrespective of tide phase and moon age has seldom been reported from the scarid species of other localities. It is suggested that spawning in the early morning would be adaptive in species such as S. rivulatus, which migrated considerable distances (ca. 500 m) to the inshore feeding sites, in order to minimize feeding losses due to migration. For male mating tactics, pair spawning by territorial TP (terminal phase) males occurred in all 14 species, and streaking and group spawning by nonterritorial small IP (initial phase) males were seen more frequently in more abundant species. Moreover, group spawning by nonterritorial TP males, which were larger than the IP males but smaller than the territorial TP males, frequently occurred in S. rivulatus. Such mating tactics of TP males have not been reported from Scaridae.     

Stable isotope analysis indicates a lack of inter- and intra-specific dietary redundancy among ecologically important coral reef fishes

Parrotfish are critical consumers on coral reefs, mediating the balance between algae and corals, and are often categorised into three functional groups based on adult morphology and feeding behaviour. We used stable isotope analysis (δ¹³C, δ¹⁵N) to investigate size-related ontogenetic dietary changes in multiple species of parrotfish on coral reefs around Zanzibar. We compared signatures among species and functional groups (scrapers, excavators and browsers) as well as ontogenetic stages (immature, initial and terminal phase) within species. Stable isotope analysis suggests that ontogenetic dietary shifts occurred in seven of the nine species examined; larger individuals had enriched δ¹³C values, with no relationship between size and δ¹⁵N. The relationship between fish length and δ¹³C signature was maintained when species were categorised as scrapers and excavators, but was more pronounced for scrapers than excavators, indicating stronger ontogenetic changes. Isotopic mixing models classified the initial phase of both the most abundant excavator (Chlorurus sordidus) as a scraper and the immature stage of the scraper Scarus ghobban (the largest species) as an excavator, indicating that diet relates to size rather than taxonomy. The results indicate that parrotfish may show similar intra-group changes in diet with length, but that their trophic ecology is more complex than suggested by morphology alone. Stable isotope analyses indicate that feeding ecology may differ among species within functional groups, and according to ontogenetic stage within a species.     

Size assortment in mixed-species groups of juvenile-phase striped parrotfish (Scarus iserti) in The Bahamas

Striped parrotfish (Scarus iserti) often form heterospecific groups with other reef fishes. In this study, we examined the species and body size composition of these groups on reefs in The Bahamas. Groups averaged approximately 4 S.?iserti and 2 associated species, with surgeonfish (Acanthurus chirurgus and A.?bahianus), slippery dick (Halichoeres bivittatus), and bluehead wrasse (Thalassoma bifasciatum) as the most common associates. Fewer groups than expected had only 1 associate; groups with 3 or more associates were more common than expected. Both the S.?iserti and associated species tended to be closely size-matched within a group, perhaps due to benefits of size assortment in lowering predation risk. Likewise, the high frequency of groups with greater than a single associate species suggests that associates may benefit from not being the only phenotypically different individual in a group.     

Paralogs are revealed by proportion of heterozygotes and deviations in read ratios in genotyping‐by‐sequencing data from natural populations

Whole‐genome duplications have occurred in the recent ancestors of many plants, fish, and amphibians, resulting in a pervasiveness of paralogous loci and the potential for both disomic and tetrasomic inheritance in the same genome. Paralogs can be difficult to reliably genotype and are often excluded from genotyping‐by‐sequencing (GBS) analyses; however, removal requires paralogs to be identified which is difficult without a reference genome. We present a method for identifying paralogs in natural populations by combining two properties of duplicated loci: (i) the expected frequency of heterozygotes exceeds that for singleton loci, and (ii) within heterozygotes, observed read ratios for each allele in GBS data will deviate from the 1:1 expected for singleton (diploid) loci. These deviations are often not apparent within individuals, particularly when sequence coverage is low; but, we postulated that summing allele reads for each locus over all heterozygous individuals in a population would provide sufficient power to detect deviations at those loci. We identified paralogous loci in three species: Chinook salmon (Oncorhynchus tshawytscha) which retains regions with ongoing residual tetrasomy on eight chromosome arms following a recent whole‐genome duplication, mountain barberry (Berberis alpina) which has a large proportion of paralogs that arose through an unknown mechanism, and dusky parrotfish (Scarus niger) which has largely rediploidized following an ancient whole‐genome duplication. Importantly, this approach only requires the genotype and allele‐specific read counts for each individual, information which is readily obtained from most GBS analysis pipelines.     

Phylogenetic relationships and the evolution of regulatory gene sequences in the parrotfishes

Regulatory genes control the expression of other genes and are key components of developmental processes such as segmentation and embryonic construction of the skull in vertebrates. Here we examine the variability and evolution of three vertebrate regulatory genes, addressing issues of their utility for phylogenetics and comparing the rates of genetic change seen in regulatory loci to the rates seen in other genes in the parrotfishes. The parrotfishes are a diverse group of colorful fishes from coral reefs and seagrasses worldwide and have been placed phylogenetically within the family Labridae. We tested phylogenetic hypotheses among the parrotfishes, with a focus on the genera Chlorurus and Scarus, by analyzing eight gene fragments for 42 parrotfishes and eight outgroup species. We sequenced mitochondrial 12s rRNA (967 bp), 16s rRNA (577 bp), and cytochrome b (477 bp). From the nuclear genome, we sequenced part of the protein-coding genes rag2 (715 bp), tmo4c4 (485 bp), and the developmental regulatory genes otx1 (672 bp), bmp4 (488bp), and dlx2 (522 bp). Bayesian, likelihood, and parsimony analyses of the resulting 4903 bp of DNA sequence produced similar topologies that confirm the monophyly of the scarines and provide a phylogeny at the species level for portions of the genera Scarus and Chlorurus. Four major clades of Scarus were recovered, with three distributed in the Indo-Pacific and one containing Caribbean/Atlantic taxa. Molecular rates suggest a Miocene origin of the parrotfishes (22 mya) and a recent divergence of species within Scarus and Chlorurus, within the past 5 million years. Developmentally important genes made a significant contribution to phylogenetic structure, and rates of genetic evolution were high in bmp4, similar to other coding nuclear genes, but low in otx1 and the dlx2 exons. Synonymous and non-synonymous substitution patterns in developmental regulatory genes support the hypothesis of stabilizing selection during the history of these genes, with several phylogenetic regions of accelerated non-synonymous change detected in the phylogeny.     

Discriminating causes from consequences of persistent parrotfish corallivory

A detailed understanding of the dual role of parrotfish as both key herbivores and potentially important corallivores is essential to the study of coral health and reef trophodynamics. Some Caribbean parrotfish regularly consume live coral, and discriminate both among coral species and among colonies within a particular species. While they prefer Montastraea spp. corals, which are dominant Caribbean reef builders, causes of selective and persistent grazing of certain colonies remain unknown. We manipulated coral exposure to parrotfish grazing through a long-term cage exclusion experiment in Belize, comparing initially grazed vs. intact (non-grazed) Montastraea spp. colonies. We measured nutrition-related characteristics (C:N ratio, %C, and %N) as well as defensive characteristics (nematocyst density and skeletal hardness) to determine if any of these variables accurately predicted parrotfish grazing. There were substantial reductions in coral nutritional quality (C:N) associated with parrotfish grazing, although these changes appear to be a consequence rather than a cause of parrotfish selectivity. Likewise, nematocyst densities were suppressed in grazed corals, also likely a result of chronic grazing stress. We found no intraspecific differences in skeletal hardness related to grazing. These results provide further demonstration of the physiological consequences of grazing, but the cause of preferential grazing by parrotfishes on certain Montastraea spp. colonies still requires further investigation.     

Cleaner fish, Labroides dimidiatus, diet preferences for different types of mucus and parasitic gnathiid isopods

Cleaner fish, Labroides dimidiatus, prefer the mucus of the parrotfish, Chlorurus sordidus, to parasitic gnathiid isopods, the main items in their diet, indicating a major conflict between clients and cleaners over what the latter should eat during interactions. We tested whether the conflict varied with client species (and the quality of its mucus) and with the presence of blood in the gnathiids. First, we offered cleaners the choice between mucus of the parrotfish and that of the snapper, Lutjanus fulviflamma. When offered equal amounts of mucus on Plexiglas plates, cleaners readily developed a significant preference for the parrotfish mucus. Reducing the amount of parrotfish mucus by 75% made the preference disappear. In a second test, we offered the cleaners gnathiids that were or were not engorged with client fish blood. Cleaners showed no significant preference for either food item. Our results suggest that the degree of conflict between cleaners and clients may vary between species, depending on whether the latter have a preferred mucus. In contrast, the cleaners' lack of preference for engorged gnathiids benefits clients because it means that cleaners do not hesitate to eat unengorged gnathiids before the gnathiids harm the fish by removing blood or by transmitting blood parasites.