Specialized Feeding Mode Research Articles

Comparison of population structure, vertical distribution and growth of sympatric, carnivorous, mesopelagic copepods,Paraeuchaeta glacialisandHeterorhabdus norvegicus, in the western Arctic Ocean

AbstractIn the Arctic Ocean, the life cycles of interzonal omnivorous copepods have been studied, whereas little information is available on the life cycles of mesopelagic carnivorous species. Here, the life cycles of two mesopelagic carnivorous copepods (Paraeuchaeta glacialis and Heterorhabdus norvegicus) are described from vertically stratified samples collected at an annual ice-station (SHEBA) in the western Arctic Ocean during 1996–1997. Reproduction estimated to occur between January and March for both species. Vertical distributions and population growth varied between the species. Early copepodite stages and adult males of P. glacialis were distributed in deeper layers, whereas late copepodite stages and adult females were observed in shallower layers. The skewed sex ratio towards females was observed for adults, which may be related to the cease feeding and short longevity for adult males. In contrast, all the H. norvegicus life stages were distributed in the mesopelagic layer. Clear peaks of the young stages and their sequence suggest that H. norvegicus may complete its life cycle within 1 year. A specialized feeding mode (incorporating a venomous injection spine and large beak) could be a key trait facilitating the achievement of rapid growth in H. norvegicus in the food-limited mesopelagic layer.

Trophic separation in planktivorous reef fishes: a new role for mucus?

The feeding apparatus directly influences a species' trophic ecology. In fishes, our understanding of feeding modes is largely derived from studies of rigid structures (i.e. bones, teeth, gill rakers). A recently described lip innovation, however, highlighted the role of soft anatomy in enabling specialized feeding modes. In this study, we explore whether similar diversification may also occur in the soft anatomy of the buccal cavity. Using four key anatomical traits to classify 19 species (14 genera) of wrasses, we evaluated the relationship between anatomical specialization of the buccal cavity and diet. Our data revealed a previously undocumented anatomical adaptation in the mouths of fairy wrasses (Cirrhilabrus): the mucosa throughout the buccal cavity (i.e. anterior to the pharynx) is packed with goblet cells, enabling it to secrete large quantities of mucus in this region; a new trait that, until now, had not been documented in wrasses. This disparity reflects diet differences, with mucus secretion found only in planktivorous Cirrhilabrus that feed predominantly on amorphous organic material (potentially gelatinous organisms). This suggests a cryptic mucus-based resource partitioning in planktivorous wrasses.

Trophic evolution in African citharinoid fishes (Teleostei: Characiformes) and the origin of intraordinal pterygophagy

The African freshwater suborder Citharinoidei (Characiformes) includes 110 species that exhibit a diversity of feeding modes comparable to those characteristic of more speciose groups such its sister, the Characoidei (2000+ species) or the distantly related Cichlidae (1600+ species). Feeding habits of the Citharinoidei range from generalist omnivores to highly specialized feeding modes including ectoparasitic fin-eating, i.e. pterygophagy. We examine diet preference evolution in the Citharinoidei using newly inferred multi-gene-based hypotheses of phylogenetic relationships for representatives of 12 of the 15 genera in the suborder. Ancestral character state reconstructions onto our best tree indicate that the three most-generalist diets - pelophage/planktivore, omnivore and invertivore - are also the most primitive conditions within the Citharinoidei. The feeding mode of the most recent common ancestor of the Citharinoidei was characterized by high uncertainty. The more specialized feeding habits - herbivory, piscivory and pterygophagy - originated later in the Citharinoidei, likely from invertivore ancestors and possibly across a short time period. Highly specialized fin eaters (Belonophago, Phago and Eugnatichthys) share a common origin along with a strict piscivore (Mesoborus) and an invertivore (Microstomatichthyoborus). The largely piscivorous, but facultative fin eater, Ichthyborus is not exclusively related to them. Our results demonstrate that overall diet preference transitions in the Citharinoidei were rare events with very few reversals or parallelisms, and that evolutionary shifts in trophic ecology have not played a major role in intraordinal diversification. This situation contrasts with other groups in which dietary transitions have played key roles in species diversification.

Morphometric-palaeoecological discrimination between Bison populations of the western Palaearctic

The present study outlines a comprehensive chrono-spatial framework of the palaeoecological adaptations among several western Palaearctic Bison populations. Possibly arrived during the middle early Pleistocene (late Villafranchian), bisons were present with various morphotypes for more than 1.5 million years in the European mammalian palaeocommunities. Based on dental wear and postcranial morphological traits, bisons can be attributed to distinct size classes and shape trends, associated with distinct feeding and locomotor adaptations across regional provinces and time intervals. During the progressively cooler and more arid climate conditions towards the late Pleistocene, a body mass increase and a significant distal limb elongation are recorded. After the last glacial climatic deterioration, the restoration of a more temperate climate and the expansion of woodlands triggered the general size decrease and limb shortening towards the beginning of the Holocene, both reflected in extant Holarctic bisons. The phenotypic diversity, imprinted in further limb structure alterations, was driven by climatic instability and landscape vegetational heterogeneity. The morphological variability among early Pleistocene forms can be attributed to evolutionary processes or most likely multiple Bison invasions at that time. The vast majority of Pleistocene European bisons primarily inhabited relatively open and dry environments, suited for grazing though they were able to exploid a variety of open and fairly wooded habitats, consuming a broad vegetational spectrum. In contrast, the increasing arid character of the southeastern part of Epivillafranchian Europe resulted in periodically harsh substrate and a more grazing specialized feeding mode.

Production of dissolved organic carbon by Oithona nana (Copepoda: Cyclopoida) grazing on two species of dinoflagellates

Production of dissolved organic carbon (DOC) by sloppy feeding copepods may represent an important source of DOC in marine food webs. By using the 14C-labeling technique, we quantify for the first time the production of DOC by the small cyclopoid copepod Oithona nana on two species of dinoflagellates, Oxyrrhis marina and Karlodinium sp. We found significant production of DOC when O. nana grazed on O. marina, corresponding to 6–15 % of the carbon ingested. When grazing the smaller Karlodinium sp., no DOC was produced. In additional experiments, we compared O. nana feeding rates on the dinoflagellate species Prorocentrum micans, Akashiwo sanguinea, Karlodinium sp. and O. marina. Clearance rates varied with prey size, with highest and lowest clearance rates on O. marina and Karlodinium sp., respectively. Our study indicates that even though O. nana feed efficiently on dinoflagellates, some of the carbon cleared can be lost as DOC. However, the DOC production by O. nana was lower than rates reported for calanoid copepods. We hypothesize that this is a result of the ambush feeding behavior of O. nana, which is considered a more specialized feeding mode than, for instance, suspension feeding. Due to high abundances and global distribution, we suggest that Oithona can represent an important source of DOC in marine ecosystems. This would particularly be the case during autumn and winter, where they may contribute to maintaining the microbial loop activities during periods of low primary production.

The Craniolingual Morphology of Waterfowl (Aves, Anseriformes) and Its Relationship with Feeding Mode Revealed Through Contrast-Enhanced X-Ray Computed Tomography and 2D Morphometrics

Within Anseriformes, waterfowl (ducks, geese, and swans) exhibit three specialized feeding modes that are distinctive among Aves: filter-feeding with fine and dense keratinous lamellae on a flat, mediolaterally expanded bill; cropping or grazing vegetation with large and robust lamellae with a dorsoventrally expanded bill; and sharp lamellae associated with a narrow bill used in acquiring mixed invertebrates and fish underwater mainly by grasping. Here we assess morphometric variation in cranial and hyolingual structures as well as hyolingual myology in a diverse sample of Anatidae to explore the relationship of tongue variation and feeding mode. Phylogenetically informed principal component analysis (phyl.PCA) of cranial-lingual measurements for 67 extant and two extinct anatids recovers grazers and filter-feeding taxa in largely distinct areas of morphospace, while underwater graspers and other mixed feeders show less distinct clustering. The relationship between morphometric differences in skeletal features and muscular variation was further explored through a reassessment of hyolingual musculature enabled by contrast-enhanced X-ray computed tomography (CT) imagery acquired from three exemplar species (Branta canadensis, Chen caerulescens, and Aythya americana) with distinctive ecologies and morphologies of the bony hyoid. Data for these duck and geese exemplars reveal further significant, and previously unstudied, morphological differences between filter-feeding and grazing species. Grazers have a larger hyolingual apparatus with highly-developed extrinsic hyoid muscles; while filter-feeding species are characterized by relatively more diminutive extrinsic hyoid muscles and larger intrinsic hyoid muscles. The feeding modes of two extinct taxa (i.e., Presbyornis and Thambetochen) were also estimated from morphometric data. The results indicate a derived terrestrial browsing or grazing ecology for Thambetochen but do not unequivocally support a specialized filter-feeding ecology for Presbyornis, which is recovered with mixed feeders including swans. The combination of detailed, CT-mediated acquisition of fine muscular anatomy with morphometric approaches shows promise for illuminating form–function relationships in extant taxa more generally.

Early development and orientation of the acoustic funnel provides insight into the evolution of sound reception pathways in cetaceans.

Whales receive underwater sounds through a fundamentally different mechanism than their close terrestrial relatives. Instead of hearing through the ear canal, cetaceans hear through specialized fatty tissues leading to an evolutionarily novel feature: an acoustic funnel located anterior to the tympanic aperture. We traced the ontogenetic development of this feature in 56 fetal specimens from 10 different families of toothed (odontocete) and baleen (mysticete) whales, using X-ray computed tomography. We also charted ear ossification patterns through ontogeny to understand the impact of heterochronic developmental processes. We determined that the acoustic funnel arises from a prominent V-shaped structure established early in ontogeny, formed by the malleus and the goniale. In odontocetes, this V-formation develops into a cone-shaped funnel facing anteriorly, directly into intramandibular acoustic fats, which is likely functionally linked to the anterior orientation of sound reception in echolocation. In contrast, the acoustic funnel in balaenopterids rotates laterally, later in fetal development, consistent with a lateral sound reception pathway. Balaenids and several fossil mysticetes retain a somewhat anteriorly oriented acoustic funnel in the mature condition, indicating that a lateral sound reception pathway in balaenopterids may be a recent evolutionary innovation linked to specialized feeding modes, such as lunge-feeding.

Early beak development in Argonauta Nodosa and Octopus Vulgaris (Cephalopoda: Incirrata) paralarvae suggests adaptation to different feeding mechanisms

Morphological and morphometric development of the beak of Argonauta nodosa (oceanic species) and Octopus vulgaris (neritic species) paralarvae were analyzed in order to verify whether or not they are determined by distinct life strategies and habitats. Measurements were taken from the upper jaw (UJ) and lower jaw (LJ), compared by the t test to identify-specific differences, and correlated with mantle length (ML) by multiple linear regression to determine overall and relative influences on growth. The jaws of both species were fragile, lightly colored, presented dentition and a slit (division) in the LJ rostrum, and showed considerable variation in general aspect. The hood and lateral walls (UJ) and crest and wings (LJ) showed the highest correlation with paralarval size (ML), and were more developed in A. nodosa than in O. vulgaris of similar size. The rostrum of O. vulgaris seems to be less functional than that of A. nodosa. The presence of beak characteristics from ancestral cephalopod species in the jaws of early paralarvae, namely teeth and a slit in the LJ rostrum, and also the inability of small-sized A. nodosa paralarvae to close the jaws and bite off a piece of prey, seem to be related to the performance of external pre-digestion and suction of body fluids of prey, a specialized feeding mode.

Beak development of early squid paralarvae (Cephalopoda: Teuthoidea) may reflect an adaptation to a specialized feeding mode

Morphological and morphometric development of the upper jaw (UJ) and lower jaw (LJ) and arm crown of Chiroteuthis cf. veranyi, Liocranchia reinhardti (oceanic species), and Doryteuthis opalescens (neritic species) paralarvae were analyzed in order to verify whether or not they are determined by developmental modes. Jaw measurements were taken, correlated with mantle length (ML) by multiple linear regression to determine relative influences on growth, and compared between species by ANOVA to identify differences. Development was expected to be similar between oceanic species, but was morphologically similar between L. reinhardti and D. opalescens, and morphometrically similar between the latter and C. cf. veranyi. UJ and LJ measurements with highest correlation with ML are larger in L. reinhardti, indicating greater beak development in this species. Rostrum robustness is higher in L. reinhardti, intermediate in D. opalescens, and lower in C. cf. veranyi, hinting at the respective prey type. Teeth (LJ) and slit, characteristics of ancestral cephalopods, are present, disappearing completely and partially on the largest specimens of L. reinhardti and D. opalescens, respectively, and remaining in all sizes of C. cf. veranyi. The results suggest that their presence in early paralarvae reflects an adaptation to sucking the pre-digested internal fluids of prey.

Specialized Feeding Modes Promote Coexistence of Competing Herbivores: Insights From a Metabolic Pool Model

Competition theory suggests that a single resource should support one consumer species. However, competitive exclusion may be relaxed by periodic disturbances, temporal or spatial segregation of consumers, or fine-scale resource partitioning. This last mechanism may be especially common for competing phytophagous insects. Unlike many predators, herbivores rarely consume their entire prey item and often have specialized feeding modes on specific plant parts. Thus, different herbivore guilds may "avoid" each other, thereby facilitating their coexistence. I analyzed a simplified metabolic pool model that includes two herbivore types: a "leaf chewer" and a "phloem feeder." Phytophagous insects with the same feeding mode never coexisted, but different guilds may coexist stably-depending on productivity of the carbohydrate pool, allocation to vegetative biomass, and defoliation rate. Differences in herbivore feeding mode are equivalent to fine scale resource partitioning, potentially within the individual plant. Thus, the addition of physiological detail changes the predictions of simple competition models and is relevant to weed biocontrol by informing decisions on which guilds of biocontrol agents to introduce.

Dating the evolutionary origins of wrasse lineages (Labridae) and the rise of trophic novelty on coral reefs

We estimated ages of divergence between major labrid tribes and the timing of the evolution of trophic novelty. Sequence data for 101 labrid taxa and 14 outgroups consisting of two mitochondrial gene regions (12s, 16s), and two nuclear protein-coding genes (RAG2, TMO4c4), a combined 2567 bp of sequence, were examined using novel maximum likelihood, maximum parsimony and mixed model Bayesian inference methods. These analyses yielded well supported trees consistent with published phylogenies. Bayesian inference using five fossil calibration points estimated the minimum ages of lineages. With origins in the late Cretaceous to early tertiary, the family diversified quickly with both major lineages (hypsigenyine and julidine) present at approximately 62.7 Ma, shortly after the K/T boundary. All lineages leading to major tribes were in place by the beginning of the Miocene (23 Ma) with most diversification in extant lineages occurring within the Miocene. Optimisation of trophic information onto the chronogram revealed multiple origins of novel feeding modes with two distinct periods of innovation. The Palaeocene/Eocene saw the origins of feeding modes that are well represented in other families: gastropod feeders, piscivores and browsing herbivores. A wave of innovation in the Oligocene/Miocene resulted in specialized feeding modes, rarely seen in other groups: coral feeding, foraminifera feeding and fish cleaning. There is little evidence of a general relationship between trophic specialization and species diversity. The current trophic diversity of the Labridae is a result of the accumulation of feeding modes dating back to the K/T boundary at 65 Ma, with all major feeding modes on present day reefs already in place 7.5 million years ago.

A New Miocene Sirenian from Kutch, India

We report a new Miocene sirenian from District Kutch, State of Gujarat, India: Domingia sodhae gen. et sp. nov. The new species is a dugongine dugongid with flattened tusk-like upper incisors. Like some other Miocene dugongids, Domningia is large and has complex, bilophodont molars and three-rooted premolars, which are strongly worn. The rostrum is downturned significantly, similar to modern dugongs, and indicative of a specialized feeding mode. Phylogenetically, it is closely related to Dioplotherium, Rytiodus, Corystosiren, and Bharatisiren. Among these, Domningia is most similar to Bharatisiren indica and Dioplotherium manigaulti, in that all three taxa retain multi-rooted premolars. Similar to Bharatisiren, the nasal process of the premaxilla is long. Bharatisiren and Domningia are part of a late Oligocene and early Miocene radiation of dugongines in South Asia.

Pisodonophis boro (ophichthidae: anguilliformes): Specialization for head‐first and tail‐first burrowing?

The rice paddy eel, Pisodonophis boro (P. boro), is of special interest because of its peculiar burrowing habits. P. boro penetrates the substrate tail-first, a technique common for ophichthids, but it is able to burrow head-first as well. P. boro exhibits three feeding modes: inertial feeding, grasping, and spinning. Rotational feeding is a highly specialized feeding mode, adopted by several elongate, aquatic vertebrates and it is likely that some morphological modifications are related to this feeding mode. The detailed morphology of the head and tail of P. boro is examined with the goal to apportion the anatomical specializations among head-first burrowing, tail-first burrowing, and rotational feeding. The reduced eyes, covered with thick corneas may be beneficial for protection during head-first burrowing, but at the same time decreased visual acuity may have an impact on other sensory systems (e.g. cephalic lateral line system). The elongated and pointed shape of the skull is beneficial for substrate penetration. The cranial bones and their joints, which are fortified, are advantageous for resisting high mechanical loads during head-first burrowing. The aponeurotic connection between epaxial and jaw muscles is considered beneficial for transferring these forces from the body to the head during rotational feeding. Hypertrophied jaw muscles facilitate a powerful bite, which is required to hold prey during spinning movements and variability in the fiber angles of subdivisions of jaw muscles may be beneficial for preventing the lower jaw from being dislodged or opened. Furthermore, firm upper (premaxillo-ethmovomerine complex) and lower jaws (with robust coronoid processes) and high neurocranial rigidity are advantageous for a solid grip to hold prey during rotational feeding. The pointed shape of the tail and the consolidated caudal skeleton are beneficial for their tail-first burrowing habits. It is quite likely that the reduction of the caudal musculature is related to the tail-first burrowing behavior because the subtle movements of the caudal fin rays are no longer required.