Digestive enzyme activities in herbivorous and carnivorous prickleback fishes (Teleostei: Stichaeidae): ontogenetic, dietary, and phylogenetic effects

We measured the activities of eight digestive enzymes in four species of herbivorous and carnivorous prickleback fishes and determined the effects of ontogeny, diet, and phylogeny on these enzyme activities. Of the four species, Cebidichthys violaceus and Xiphister mucosus shift to a more herbivorous diet as they grow (> or =45 mm SL [standard length]), whereas Xiphister atropurpureus and Anoplarchus purpurescens remain carnivores throughout life. Digestive enzyme activities of small (30-40 mm SL) carnivorous juveniles were compared with those of larger (60-75 mm SL) wild-caught juveniles that had consumed a natural diet and larger (60-75 mm SL) juveniles raised on a high-protein animal diet. Cebidichthys violaceus and both species of Xiphister showed ontogenetic changes in digestive enzyme activities, whereas A. purpurescens did not. Despite dietary differences between X. atropurpureus and X. mucosus, these sister taxa displayed the most similar digestive enzyme activities from ontogenetic and dietary perspectives (high alpha-amylase and lipase and low trypsin and aminopeptidase activities), and both were more similar to C. violaceus, a member of the same largely herbivorous clade, than either was to A. purpurescens, a member of an adjacent, carnivorous clade. The results support the hypothesis that phylogeny influences digestive enzyme activities in these fishes. Anoplarchus purpurescens, a carnivore with a diverse diet, showed great plasticity in enzyme activity, especially trypsin and aminopeptidase, which were elevated in this species to the highest level among the four species after consuming the high-protein diet. These results support the hypothesis that fishes with relatively broad diets can modulate digestive enzyme activities in response to changes in dietary composition.     

More than one way to be an herbivore: convergent evolution of herbivory using different digestive strategies in prickleback fishes (Stichaeidae)

In fishes, the evolution of herbivory has occured within a spectrum of digestive strategies, with two extremes on opposite ends: (i) a rate-maximization strategy characterized by high intake, rapid throughput of food through the gut, and little reliance on microbial digestion or (ii) a yield-maximization strategy characterized by measured intake, slower transit of food through the gut, and more of a reliance on microbial digestion in the hindgut. One of these strategies tends to be favored within a given clade of fishes. Here, we tested the hypothesis that rate or yield digestive strategies can arise in convergently evolved herbivores within a given lineage. In the family Stichaeidae, convergent evolution of herbivory occured in Cebidichthys violaceus and Xiphister mucosus, and despite nearly identical diets, these two species have different digestive physiologies. We found that C. violaceus has more digesta in its distal intestine than other gut regions, has comparatively high concentrations (>11 mM) of short-chain fatty acids (SCFA, the endpoints of microbial fermentation) in its distal intestine, and a spike in β-glucosidase activity in this gut region, findings that, when coupled to long retention times (>20 h) of food in the guts of C. violaceus, suggest a yield-maximizing strategy in this species. X. mucosus showed none of these features and was more similar to its sister taxon, the omnivorous Xiphister atropurpureus, in terms of digestive enzyme activities, gut content partitioning, and concentrations of SCFA in their distal intestines. We also contrasted these herbivores and omnivores with other sympatric stichaeid fishes, Phytichthys chirus (omnivore) and Anoplarchus purpurescens (carnivore), each of which had digestive physiologies consistent with the consumption of animal material. This study shows that rate- and yield-maximizing strategies can evolve in closely related fishes and suggests that resource partitioning can play out on the level of digestive physiology in sympatric, closely related herbivores.     

Digestive enzyme activities in carnivores and herbivores: comparisons among four closely related prickleback fishes (Teleostei: Stichaeidae) from a California rocky intertidal habitat

Three digestive enzymes in four species of closely related prickleback fishes (family Stichaeidae: Cebidichthys violaceus, Xiphister mucosus , Xiphister atropurpureus and Anoplarchus purpurescens ) were analysed to assess whether diet or phylogeny played a larger role in influencing digestive enzyme activity. Cebidichthys violaceus and X. mucosus are primarily herbivorous, whereas X. atropurpureus and A. purpurescens are mainly carnivorous. The two Xiphister species are sister taxa, and A. purpurescens is in a clade adjacent to that of the three other species. Pepsin and trypsin specific activities did not differ significantly among the four species, but α‐amylase activity was significantly higher in the two Xiphister species, followed by C. violaceus , and then A. purpurescens . The wide disparity between the two carnivores, the striking similarity between the two sister taxa, and the significant difference between the two herbivores indicate that activity of α‐amylase follows a pattern influenced more by phylogeny than by diet in these fishes.     

Guild structure of carnivorous intertidal fishes of the Chilean coast: implications of ontogenetic dietary shifts

Although ontogenetic changes in resource use within species are common in animals, these changes have not been widely considered in studies of guild structure within communities. The occurrence of one or more shifts in resource use in an individual of a given species during its life should mean that it would also belong to different guilds at different life stages. We specifically addressed this issue by describing the feeding habits of ten species of carnivorous fishes occurring in tidepools in rocky intertidal areas along the coast of central Chile. Most of these species undergo clear ontogenetic dietary shifts and a feeding guild structure of this group of fishes was established that takes these dietary shifts into account. Each species was divided into a number of size classes. Dietary overlap values between both intraspecific and interspecific size-class pairs in the entire group of ten species were used to construct a phenogram of dietary similarity through an UPGMA cluster analysis. Numbers of guilds and their memberships were established objectively by applying a bootstrapping procedure. Four “ontogenetic” feeding guilds (OFGs), each consisting of size-classes of species, were recognized. The majority of species belonged to more that one guild. Interestingly, when the bootstrapping procedure was applied to a phenogram based on the diets of “taxonomic” or complete species, only one significant guild was found. The implications of these ontogenetic dietary shifts for interspecific interactions are substantial because the identity of the species with which each fish species shares resources change through their lives. The usefulness of taxonomic species for investigating potential competitive interactions in this assemblage is greatly undermined. Received: 26 September 1997 / Accepted: 15 December 1997     

Reproductive biology and female parental care in the cockscomb prickleback,Anoplarchus purpurescens (Pisces: Stichaeidae)

Synopsis Reproduction and parental care in the cockscomb prickleback, a Pacific coast intertidal fish, were examined using a combination of field and laboratory observations. The sexes were dimorphic, particularly during the breeding season, and males competed with other males for access to females. Males performed lateral and spasm displays. In the wild, the breeding season extended from January to March on cobblestone beaches. Assortative mating was positive with respect to body size. Females exhibited solitary parental care of the eggs. Each female coiled around, guarded and fanned a single egg mass that likely represented her total reproductive effort for the year. The number of eggs in the mass increased linearly with female size (weight or length). Males did not remain after spawning. Aquarium observations revealed that males spawn with more than one female given the opportunity. It is not known whether this occurs in the wild. Incubation to hatching took 29 days. Upon hatching, the young swam towards the surface. Parental care did not extend beyond hatching.     

A new genus and species of prickleback (Perciformes: Stichaeidae) from Japan

A stichaeid fish, Xenolumpenus longipterus gen. et sp. nov., is described on the basis of 2 specimens (107.1–114.9 mm in standard length) collected from 167 to 300 m in the northern Sea of Japan off southern Hokkaido, Japan. Xenolumpenus is unique among all known genera of the subfamily Lumpeninae in having all pectoral, pelvic, and anal fin rays elongate and unbranched with fin membranes well-incised. Xenolumpenus longipterus can be further distinguished from all species of the subfamily in having the following combination of characters: dorsal fin XLVI–XLVIII; anal fin II, 28–29; pectoral fin 11; large black blotches on pectoral fin; and black ocellus on caudal fin.     

Comparative osteology and phylogenetic systematics of fossil and living bony-tongue fishes (Actinopterygii, Teleostei, Osteoglossomorpha)

Several recent studies using analyses of morphological characters have addressed the interrelationships of Osteoglossomorpha, a group that sometimes is considered the living sister group of all other living teleosts. Many characters used in these studies were found to be poorly defined, to be coded incorrectly or illogically, or to display more variation than was described. The goal of this study is to address these concerns and contribute generally to knowledge of the morphology and systematic relationships of osteoglossomorphs. Analysis of 72 characters (65 informative) scored for 20 genera resulted in two most parsimonious cladograms (171 steps, CI = 0.6433, CI = 0.6139 excluding uninformative characters, HI = 0.3977, HI = 0.3861 excluding uninformative characters; RI = 0.7782; RC = 0.5006). Osteoglossomorpha is supported by both synapomorphies and homoplasies, although its monophyly was not truly tested in this analysis (only a single outgroup, Elops , was included in the analysis). The only difference in the topologies of these cladograms is in the position of ?Lycoptera (recovered as either the sister group of all other osteoglossomorphs sampled or of ?Eohiodon +Hiodon ). ?Ostariostoma is recovered as the sister group of all non‐hiodontiform osteoglossomorphs. Mormyrids are the sister group of notopterids + osteoglossids. This clade has not been found in other recent analyses. Mormyrids and notopterids usually are considered more closely related to each other than to any other group; characters not included here support this relationship and future consideration of these characters must be made. Although almost completely dichotomous, many nodes of the resulting trees lack rigorous support. For example, ?Palaeonotopterus is interpreted as the sister group of all mormyrids sampled, although for this taxon only 22% of characters could be scored. © 2003 The Linnean Society of London. Zoological Journal of the Linnean Society , 2003, 137 , 1?100.     

Genus Leptostichaeus and its position in the taxonomy of fishes (Perciformes: Zoarcoidei, Stichaeidae)

Up to the present, the genus Leptostichaeus has been considered as belonging to subfamily Lumpeninae. A series of characters was analyzed for family and subfamily diagnostics within the group Stichaeidae. It was found that, in combination of all examined characters, the genus Leptostichaeus is either similar to Azygopterus or occupies an intermediate position between the latter and other members of the family Stichaeidae. The genus Leptostichaeus is transferred into the group Azygopterinae, which is revalidated as a subfamily within the family Stichaeidae.     

Morphology and ontogeny of multiple lateral‐line canals in the rock prickleback,Xiphister mucosus (Cottiformes: Zoarcoidei: Stichaeidae)

The structure and ontogeny of lateral‐line canals in the Rock Prickleback, Xiphister mucosus, were studied using cleared‐and‐stained specimens, and the distribution and morphology of neuromasts within lateral‐line canals were examined using histology. X. mucosus has seven cephalic canals in a pattern that, aside from four branches of the infraorbital canals, is similar to that of most teleostean fishes. Unlike most other teleosts, however, X. mucosus features multiple trunk lateral‐line canals. These include a short median posterior extension of the supratemporal canal and three paired, branching canals located on the dorsolateral, mediolateral, and ventrolateral surfaces. The ventrolateral canal (VLC) includes a loop across the ventral surface of the abdomen. All trunk canals, as well as the branches of the infraorbitals, are supported by small, dermal, ring‐like ossifications that develop independently from scales. Trunk canals develop asynchronously with the mediodorsal and dorsolateral canals (DLC) developing earliest, followed by the VLC, and, finally, by the mediolateral canal (MLC). Only the mediodorsal and DLC connect to the cephalic sensory canals. Fractal analysis shows that the complexity of the trunk lateral‐line canals stabilizes when all trunk canals develop and begin to branch. Histological sections show that neuromasts are present in all cephalic canals and in the DLC and MLC of the trunk. However, no neuromasts were identified in the VLC or its abdominal loop. The VLC cannot, therefore, directly function as a part of the mechanosensory system in X. mucosus. The evolution and functional role of multiple lateral‐line canals are discussed. J. Morphol. 276:1218–1229, 2015. © 2015 Wiley Periodicals, Inc.     

Assimilation of carbon from dietary and nondietary macroalgae by a temperate-zone intertidal fish, Cebidichthys violaceus (Girard) (Teleostei: Stichaeidae)

Force-feeding experiments were performed to measure the assimilation of carbon by the herbivorous stichaeid fish Cebidichthys violaceus (Girard) from macroalgae either regularly consumed or avoided by the fish. Dietary species were the green alga Ulva lobata (Kütz.) S. & G. and the red algae Porphyraperforata J. Ag. and Iridaea flaccida (S. & G.) Silva while the nondietary species were the brown algae Macrocystis integrifolia Bory and Fucus distichus (de la Pyl.) Pow. ¹⁴C was found in five body compartments (stomach, intestine, liver, carcass and skin) of fish fed labeled portions of Ulva lobata, Porphyra perforata and Macrocystis integrifolia. Approximately equal amounts of ¹⁴C were assimilated from diatom-free thalli of Ulva lobata that were either untreated or treated with antibiotics to remove bacterial populations. Labeled carbon was also assimilated from bacteria- and diatom-free thalli of Iridaea flaccida, Macrocystis integrifolia and Fucus distichus. Assimilation efficiencies of unlabeled carbon (determined from CHN analyses of food and feces) varied widely among the dietary and nondietary algae. The markedly lower levels of carbon assimilation from the brown algae may be due to reduced digestibility of their carbohydrates and, for F. distichus, the presence of secondary compounds. The results of this study clearly show that a temperate marine fish can assimilate carbon from taxonomically diverse algae largely free of epibionts.     

Trophic biology of herbivorous reef fishes: alimentary pH and digestive capabilities

Certain herbivorous fishes are well known for morphological specializations enabling trituration; such as scarids with a pharyngeal mill and mullets with a gizzard-like stomach. However, utilization of plant foods by fishes is limited by these animal's digestive capabilities, most notably the apparent lack of cellulose digesting enzymes. Fishes possessing a grinding mechanism are able to break open plant cells for digestion. But how fishes without grinding mechanisms make plant cell contents accessible to digestion is unknown. These fishes include many acanthurid and pomacentrid species which are among the most abundant on reefs. Another mechanism for rupturing plant cell walls has been recently proposed, namely lysis by gastric acidity. This study surveyed stomach and intestinal pH for 17 herbivorous species at Fanning Atoll, Central Pacific and two species from St Croix, Caribbean with additional data for seven selected carnivorous species. The herbivorous fishes included acanthurids (surgeonfishes), mugilids (mullets), pomacanthids (angelfishes), pomacentrids (damselfishes) and a scarid (parrotfish). The effect of different pH concentrations and trituration was examined experimentally for eight common Pacific marine algae including two reds, two blue-greens, two greens, one brown, and the algal mat complex from inside damselfish territories. Fishes, possessing morphological adaptations for trituration, ingested quantities of calcium carbonate material and did not contain gastric acidity low enough to lyse algal cell wells. However, fishes without grinding mechanisms but with defined stomachs have gastric pH values from 2.4 to 4.25 which can be as effective as trituration in releasing algal cell contents of certain algae. These results are considered in a review of previous studies of herbivory in fishes. The trophic relationship between fishes and algae of specified morphologies are predicted by extrapolation from the experimental results on algae vulnerable to acid lysis or trituration.     

Multiple in-to-Africa dispersals of labeonin fishes (Teleostei: Cyprinidae) revealed by molecular phylogenetic analysis

An out-of-Africa dispersal route has been proposed for many organisms, including modern man. However, counter examples of in-to-Africa dispersal routes are less common. In the present article, the phylogenetic relationships within the Labeoninae, a subfamily of cyprinid fishes distributed in Asia and Africa, were analyzed to investigate the biogeographic processes governing the modern distribution of these Asian and African cyprinids. The mitochondrial DNA cytochrome b gene was used as a molecular marker. The phylogenetic analysis indicated that the subfamily Labeoninae is a monophyletic group, with some Asian labeonins located at the basal position. Two subclades were found that contained both African and Asian species, which highlighted a need for further biogeographic analysis. Based on this analysis, it is proposed that the centre of origin of the Labeoninae was in East Asia. Molecular clock estimation suggests that the Labeoninae arose by the Early Miocene (~23 MYA) during the period of the second Tibetan uplift. Subsequently, two dispersal events of labeonins from Asia into Africa occured in the Early Miocene (~ 20 MYA) and Late Miocene (~9 MYA) and serve as examples counter to out-of-Africa dispersal.     

Electric fishes of the genus Sternarchorhynchus (Teleostei,Ostariophysi, Gymnotiformes); phylogenetic and revisionary studies

Analysis of 88 characters of external and internal body systems yielded a phylogenetic reconstruction of the Neotropical electric knifefish genus Sternarchorhynchus (Apteronotidae; Gymnotiformes). The results support a hypothesis of Sternarchorhynchus as the sister group to Platyurosternarchus. A series of synapomorphies, many involving major innovations of the neurocranium, jaws, suspensorium, and associated systems that permit an unusual mode of grasp‐suction feeding, support the monophyly of both genera. Synapomorphies largely resolve relationships within Sternarchorhynchus with basal nodes strongly supported by characters pertinent to prey capture and initial processing of food items. These possible key innovations may provide Sternarchorhynchus with a competitive advantage over other clades of the Apteronotidae and account for the species diversity of the genus in Neotropical rivers. Adaptive radiation in Sternarchorhynchus was analysed. Habitat preference transitions repeatedly occurred in the genus between deep‐river channel dwelling species and rheophilic species with preferences for higher energy setting including rapids and swift‐flowing fluviatile settings. Twenty‐two species of Sternarchorhynchus are described as new based on samples that originated in the smaller rivers draining into the Golfo de Paria, the Marowijne and Essequibo River basins, the Río Orinoco and in particular the Amazon River basin. The 32 species in Sternarchorhynchus make it the most speciose genus in the Apteronotidae. No claim to original US government works. Journal compilation © 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 159 , 223–371.     

Interrelationships of the ostariophysan fishes (Teleostei)

The history of ostariophysan classification is summarized and it is noted that traditional concepts of relationships have never been supported by characters found to be unique to the taxa. We present a new hypothesis of relationships among four of the five major ostariophysan lineages: Cypriniformes, Characiformes, Siluroidei, and Gymnotoidei (Otophysi). Cypriniforms are the sister-group of the remaining three (Characiphysi), and characiforms are the sister-group of siluroids plus gymnotoids (Siluriformes). Placement of the Gonorynchiformes as the sister-group of the Otophysi is supported by additional evidence. Each of the five lineages is monophyletic. Analysis was concentrated upon species thought to be the least specialized within each lineage; choices of these species are discussed. Chanos is determined to be a relatively primitive gonorynchiform morphologically and the sister-group of all other Recent members of the order. Opsariichthys and Zacco are found to be morphologically primitive cypriniforms. We propose that a monophyletic group comprising the Citharinidae and Distichodontidae forms the sister-group of all other characiforms. Within the two families, Xenocharax is the least specialized. We suggest that Hepsetus, the erythrinids, and the ctenoluciids are more derived than the distichodontids and citharinids, and may form a monophyletic group within die characiforms. The traditional hypothesis that Diplomystes is the primitive sister-group of all Recent siluroids is substantiated. Our evidence suggests that Sternopygus is the most primitive gymnotoid morphologically; but rather than being the sister-group of all other gymnotoids, it is the primitive sister-group within a lineage called the Sternopygidae by Mago-Leccia. Previous explanations of otophysan distribution have been based on notions of relationships which are unsupported by the evidence presented herein. Our own analysis of relationships serves primarily to make clear the extent of sympatry, and therefore the probability of dispersal, among the major ostariophysan lineages. The extent of sympatry, together with the widespread distribution of ostariophysans, suggests that the group is older than previously supposed, and our hypotheses of relationships among the characiforms implies that many of the extent characiform lineages evolved before the separation of Africa and South America. Further understanding of ostariophysan distribution must await phylogenetic analysis within each of the five major lineages so that distributions linked with vicariance patterns and dispersal events can be sorted out.     

Apoptosis in the digestive tract of herbivorous Rana pipiens larvae and carnivorous Ceratophrys ornata larvae: An immunohistochemical study

The lifespan of herbivorous Rana pipiens larvae is ～3 months, while that of carnivorous Ceratophrys ornata larvae is only about 2 weeks. During metamorphic climax, the larval gut shortens dramatically, especially in R. pipiens, and its luminal epithelium is replaced by adult‐type epithelium. To determine when programmed cell death occurs during the metamorphic restructuring of the gut, we prepared cross‐sections of the stomach, small intestine, and large intestine from representative larval stages and from juvenile frogs of both species. The sections were incubated with monoclonal antibody against active caspase‐3, one of the key enzymes in the apoptotic cascade. We observed apoptosis in some luminal epithelial cells in each of the three regions of the larval gastrointestinal tract of both species. However, apoptotic cells appeared earlier in larval stages of R. pipiens than C. ornata and few were seen in juvenile frogs of either species. The results demonstrate the occurrence of apoptosis in the metamorphic remodeling of the gut of both R. pipiens larvae and C. ornata larvae. J. Morphol., 2011. © 2011 Wiley Periodicals, Inc.     

The evolution of pharyngeal bones and teeth in Gobioninae fishes (Teleostei: Cyprinidae) analyzed with phylogenetic comparative methods

The subfamily Gobioninae is a subgroup in the specious fish family Cyprinidae, which bears high diversity in morphological and ecological dimensions and has its most components distributed in East Asia. In this study, the pharyngeal bones and teeth of 39 species belonging to 19 genera of the Gobioninae were examined, with the phylogenetic comparative method (PCM) and correlation methods employed to analyze the character evolution. Three characters on pharyngeal bones (shape of the pharyngeal bones, extension for attachment of the pharyngo-cleithralis internus posterior (PCIP) muscle, and teeth-bearing area) and six characters of pharyngeal teeth (shape of the five teeth in the main row, number of rows of the teeth) were identified and compared. When the character states were mapped on a molecular phylogenetic tree, it was found that, to adapt to different masticatory operations, different Gobioninae species have various morphological types of pharyngeal bones and teeth: some have intermediate pharyngeal bones bearing multiple rows of diverse teeth (conical, coarsely compressed, and compressed), others have broad pharyngeal bones bearing a single row of molar teeth, and still others have narrow pharyngeal bones bearing a single row of extremely compressed teeth. Tests on the phylogenetic signal and evolutionary associations revealed that evolution of the examined characters was all phylogenetically constrained and correlated. Owing to the homoplasy in evolution, it was suggested that the conventional method of using pharyngeal bones and teeth for phylogenetic reconstruction of cyprinid fishes should not be encouraged.     

A rod-dominated visual system in leptocephalus larvae of elopomorph fishes (Elopomorpha: Teleostei)

The nature and distributions of photoreceptor cell types were investigated in the retinas of 12 species (5 families) of elopomorph anguilliform leptocephalus larvae. Anti-opsin immunofluorescence, light microscopy and transmission electron microscopy (TEM) were used to assess opsin distribution across the retinas and to associate photoreceptor morphology and opsin content. Retinas of all species were immunoreactive with anti-rhodopsin throughout, while anti-cone opsin immunoreactivity was restricted only to the ventral region of the retina in all specimens. Rod and cone photoreceptors were morphologically indistinguishable at low magnifications; TEM revealed that nearly all photoreceptors had rod-like ultrastructure, with only rare examples of cone-like cells identified in the ventral retina. These results indicate a rhodopsin/rod-dominated retina in leptocephalus larvae of anguilliform eels in the teleost subdivision Elopomorpha, contrasting with the cone-dominated retinas of nearly all other species of teleost larvae. This distinctive developmental pattern shared among elopomorph larvae has important evolutionary and ecological implications, indicating a shared ancestor and/or ecological characteristics that are very different from most other teleost larvae.