The evolution of flight and echolocation in bats: another leap in the dark

The earliest known complete bats, from the Eocene (49–53 Mya), were already capable of flapping flight and echolocation. In the absence of direct fossil evidence there have been many speculative scenarios advanced to explain the evolution of these behaviours and their distributions in extant bats. Theories assuming chiropteran monophyly have generally presumed the ancestral pre‐bat was nocturnal, arboreal and insectivorous. Following this assumption hypotheses can be divided into the echolocation first, flight first and tandem development hypotheses, all of which assume that flight evolved only once in the lineage. In contrast, the chiropteran diphyly hypothesis suggests that flight evolved twice. Evidence supporting and refuting the different hypotheses are reviewed. It is concluded that there are significant problems attached to all the current models. A novel hypothesis is advanced, which starts from the assumption that bats are monophyletic and the ancestral pre‐bat was arboreal, but diurnal and frugivorous. After the evolution of flight it is suggested that these animals were driven into the nocturnal niche by the evolution of raptorial birds, and different groups evolved either specialised nocturnal vision (megachiropterans) or echolocation (microchiropterans). A block on sensory modality transfer has retained this distribution of perceptual capabilities ever since, despite some Megachiroptera evolving rudimentary echolocation, and the dietary convergence of some Microchiroptera with the Megachiroptera. The new hypothesis overcomes many of the problems identified in previous treatments.     

The Origin and Initial Rise of Pelagic Cephalopods in the Ordovician

Background

During the Ordovician the global diversity increased dramatically at family, genus and species levels. Partially the diversification is explained by an increased nutrient, and phytoplankton availability in the open water. Cephalopods are among the top predators of todays open oceans. Their Ordovician occurrences, diversity evolution and abundance pattern potentially provides information on the evolution of the pelagic food chain.

Methodology/Principal Findings

We reconstructed the cephalopod departure from originally exclusively neritic habitats into the pelagic zone by the compilation of occurrence data in offshore paleoenvironments from the Paleobiology Database, and from own data, by evidence of the functional morphology, and the taphonomy of selected cephalopod faunas. The occurrence data show, that cephalopod associations in offshore depositional settings and black shales are characterized by a specific composition, often dominated by orthocerids and lituitids. The siphuncle and conch form of these cephalopods indicate a dominant lifestyle as pelagic, vertical migrants. The frequency distribution of conch sizes and the pattern of epibionts indicate an autochthonous origin of the majority of orthocerid and lituitid shells. The consistent concentration of these cephalopods in deep subtidal sediments, starting from the middle Tremadocian indicates the occupation of the pelagic zone early in the Early Ordovician and a subsequent diversification which peaked during the Darriwilian.

Conclusions/Significance

The exploitation of the pelagic realm started synchronously in several independent invertebrate clades during the latest Cambrian to Middle Ordovician. The initial rise and diversification of pelagic cephalopods during the Early and Middle Ordovician indicates the establishment of a pelagic food chain sustainable enough for the development of a diverse fauna of large predators. The earliest pelagic cephalopods were slowly swimming vertical migrants. The appearance and early diversification of pelagic cephalopods is interpreted as a consequence of the increased food availability in the open water since the latest Cambrian.     

Allometric patterns of fetal head growth in mysticetes and odontocetes: Comparison of Balaena mysticetus and Stenella attenuata

Unlike other mammals, odontocetes and mysticetes have highly derived craniofacial bones. A growth process referred to as “telescoping” is partly responsible for this morphology. Here, we explore how changes in facial morphology during fetal growth relate to differences in telescoping between the adult odontocete Stenella attenuata and the mysticete Balaena mysticetus. We conclude that in both Stenella and Balaena head size increases allometrically. Similarly, odontocete nasal length and mysticete mouth size have strong positive allometry compared to total body length. However, the differences between odontocetes and mysticetes in telescoping are not directly associated with their fetal growth patterns. Our results suggest that cranial changes related to echolocation and feeding between odontocetes and mysticetes, respectively, begin during ontogeny before telescoping is initiated.     

A bizarre new toothed mysticete (Cetacea) from Australia and the early evolution of baleen whales

Extant baleen whales (Cetacea, Mysticeti) are all large filter-feeding marine mammals that lack teeth as adults, instead possessing baleen, and feed on small marine animals in bulk. The early evolution of these superlative mammals, and their unique feeding method, has hitherto remained enigmatic. Here, I report a new toothed mysticete from the Late Oligocene of Australia that is more archaic than any previously described. Unlike all other mysticetes, this new whale was small, had enormous eyes and lacked derived adaptations for bulk filter-feeding. Several morphological features suggest that this mysticete was a macrophagous predator, being convergent on some Mesozoic marine reptiles and the extant leopard seal (Hydrurga leptonyx). It thus refutes the notions that all stem mysticetes were filter-feeders, and that the origins and initial radiation of mysticetes was linked to the evolution of filter-feeding. Mysticetes evidently radiated into a variety of disparate forms and feeding ecologies before the evolution of baleen or filter-feeding. The phylogenetic context of the new whale indicates that basal mysticetes were macrophagous predators that did not employ filter-feeding or echolocation, and that the evolution of characters associated with bulk filter-feeding was gradual.     

Host defense mechanisms of cephalopods

Humoral and cellular mechanisms of defense have been described for cephalopods, a relatively advanced group of mollusks. Typical of other mollusks, cephalopod agglutinins are the most documented component of humoral immunity. Lectins, which have agglutinating properties, have been described and characterized from octopuses. Agglutinins from cephalopod hemolymph have also been shown to agglutinate a variety of vertebrate red blood cells, as well as potential bacterial pathogens. Hemocytes are the primary component of cellular immunity. Although the hemocyte role in phagocytosis has been extensively studied in other mollusks, the mechanisms of phagocytosis have not been described extensively for cephalopods. Cephalopod hemocytes have phagocytic capabilities and may function in encapsulation and neutralization of foreign substances; however, the effects of environmental factors and the full extent of phagocytic capabilities of cephalopod hemocytes have not been reported. Hemocytes from cephalopods have a role in wound healing and inflammation which have been reported in detail by several investigators.     

Do man‐made structures and water depth affect the diel rhythms in click recordings of harbor porpoises (Phocoena phocoena)?

The construction of industrial offshore structures may lead to colonization by a variety of marine organisms resulting in locally enhanced biodiversity and biomass, which may then affect the habitat use and behavior of marine predators. For harbor porpoises high nocturnal echolocation activity was demonstrated near industrial structures and it was hypothesized that this was caused by increased feeding opportunities at night. Here we tested the hypothesis that bridge pillars will lead to more nocturnal echolocation activity by porpoises near them than at positions further away. The daily rhythms in porpoise detections near bridge pillars tended to be slightly more pronounced and a greater proportion of clicks occurred during the night. However, water depth had a greater impact on these rhythms, with more nocturnal porpoise echolocation activity and more pronounced daily rhythms in deeper waters. This may be related to different feeding techniques and prey choice by porpoises in deep and shallow water. In deeper water porpoises may be feeding pelagically on herring and cod, which show more activity and are easier to catch at night. In shallow water they may be targeting mainly gobies using a bottom feeding technique and this may not be more efficient at night.     

Auditory temporal resolution and evoked responses to pulsed sounds for the Yangtze finless porpoises (<Emphasis Type="Italic">Neophocaena phocaenoides asiaeorientalis</Emphasis>)

Temporal cues are important for some forms of auditory processing, such as echolocation. Among odontocetes (toothed whales, dolphins, and porpoises), it has been suggested that porpoises may have temporal processing abilities which differ from other odontocetes because of their relatively narrow auditory filters and longer duration echolocation signals. This study examined auditory temporal resolution in two Yangtze finless porpoises (Neophocaena phocaenoides asiaeorientalis) using auditory evoked potentials (AEPs) to measure: (a) rate following responses and modulation rate transfer function for 100 kHz centered pulse sounds and (b) hearing thresholds and response amplitudes generated by individual pulses of different durations. The animals followed pulses well at modulation rates up to 1,250 Hz, after which response amplitudes declined until extinguished beyond 2,500 Hz. The subjects had significantly better hearing thresholds for longer, narrower-band pulses similar to porpoise echolocation signals compared to brief, broadband sounds resembling dolphin clicks. Results indicate that the Yangtze finless porpoise follows individual acoustic signals at rates similar to other odontocetes tested. Relatively good sensitivity for longer duration, narrow-band signals suggests that finless porpoise hearing is well suited to detect their unique echolocation signals.     

How intelligent is a cephalopod? Lessons from comparative cognition

The soft-bodied cephalopods including octopus, cuttlefish, and squid are broadly considered to be the most cognitively advanced group of invertebrates. Previous research has demonstrated that these large-brained molluscs possess a suite of cognitive attributes that are comparable to those found in some vertebrates, including highly developed perception, learning, and memory abilities. Cephalopods are also renowned for performing sophisticated feats of flexible behaviour, which have led to claims of complex cognition such as causal reasoning, future planning, and mental attribution. Hypotheses to explain why complex cognition might have emerged in cephalopods suggest that a combination of predation, foraging, and competitive pressures are likely to have driven cognitive complexity in this group of animals. Currently, it is difficult to gauge the extent to which cephalopod behaviours are underpinned by complex cognition because many of the recent claims are largely based on anecdotal evidence. In this review, we provide a general overview of cephalopod cognition with a particular focus on the cognitive attributes that are thought to be prerequisites for more complex cognitive abilities. We then discuss different types of behavioural flexibility exhibited by cephalopods and, using examples from other taxa, highlight that behavioural flexibility could be explained by putatively simpler mechanisms. Consequently, behavioural flexibility should not be used as evidence of complex cognition. Fortunately, the field of comparative cognition centres on designing methods to pinpoint the underlying mechanisms that drive behaviours. To illustrate the utility of the methods developed in comparative cognition research, we provide a series of experimental designs aimed at distinguishing between complex cognition and simpler alternative explanations. Finally, we discuss the advantages of using cephalopods to develop a more comprehensive reconstruction of cognitive evolution.     

A molecular and karyological approach to the taxonomy of Nautilus

Nautiloids, the externally shelled cephalopods of Cambrian origin, are the most ancient lineage among extant cephalopods. Their ancestral characters are explored based on morphological and molecular data (18S rDNA sequence) to investigate the evolution of present cephalopod lineages. Among molluscs, nautilus 18S rDNA gene is the longest reported so far, due to large nucleotidic insertions. By comparison with other 18S sequences, the complete gene of N. macromphalus helps to clarify the taxonomic status of the three universally recognised Nautilus species. The range of interspecific molecular differences supports separation of the present species into two surviving ectocochleate genera, Nautilus and Allonautilus. Nautiloid 18S is considered as corresponding to the ancestral form of 18S as is the number of chromosomes in Nautilus (52), the lowest among cephalopods. Comparison of karyological characteristics amongst cephalopods in a phylogenetic context suggests a possible correlation between duplication events and lineage divergence.     

浙南近海头足类种类组成及生态位分析

在浙南海域布设42个调查站位,于2015年1 1月、2016年2月、5月和8月进行了4个航次的系统调查.针对获得的头足类样品,运用相对重要性指数、生态位宽度和生态位重叠等生态指标,结合非度量多维标度法(nMDS)和典范对应分析(CCA)对生态位的重叠和分化进行分析.结果 表明:调查海域有头足类14种,优势种为剑尖枪乌贼...     

Cephalopod and Groundfish Landings: Evidence for Ecological Change in Global Fisheries?

Cephalopod fisheries are among the few still with some local potential for expansion; in fact, as groundfish landings have declined globally, cephalopod landings have increased. We propose the hypothesis that, although increased cephalopod landings may partly reflect increased market demand, overfishing groundfish stocks has positively affected cephalopod populations. Data from 15 key FAO areas reveal that, with the exception of the north- east Atlantic, cephalopod landings have increased significantly over the last 25 years while groundfish have risen more slowly, remained stable, or declined. In terms of volume, cephalopods have not replaced groundfish. This is hypothesized as owing to the shorter life cycle of cephalopods, and rapid turnover and lower standing stocks than for longer-lived finfish species. Under high fishing pressure, groundfish are probably poor competitors, having less opportunity for spawning and replacement. In West Africa, the Gulf of Thailand and Adriatic there is strong circumstantial evidence that fishing pressure has changed ecological conditions and cephalopod stocks have increased as predatory fish have declined. We recommend that this hypothesis be tested thoroughly in other areas where suitable data exist. Most coastal and shelf cephalopod fisheries are likely to be fully exploited or overexploited, and current annual fluctuations in cephalopod landings are probably largely environmentally-driven.     

Experimental evidence for group hunting via eavesdropping in echolocating bats

Group foraging has been suggested as an important factor for the evolution of sociality. However, visual cues are predominantly used to gain information about group members'' foraging success in diurnally foraging animals such as birds, where group foraging has been studied most intensively. By contrast, nocturnal animals, such as bats, would have to rely on other cues or signals to coordinate foraging. We investigated the role of echolocation calls as inadvertently produced cues for social foraging in the insectivorous bat Noctilio albiventris. Females of this species live in small groups, forage over water bodies for swarming insects and have an extremely short daily activity period. We predicted and confirmed that (i) free-ranging bats are attracted by playbacks of echolocation calls produced during prey capture, and that (ii) bats of the same social unit forage together to benefit from passive information transfer via the change in group members'' echolocation calls upon finding prey. Network analysis of high-resolution automated radio telemetry confirmed that group members flew within the predicted maximum hearing distance 94±6 per cent of the time. Thus, echolocation calls also serve as intraspecific communication cues. Sociality appears to allow for more effective group foraging strategies via eavesdropping on acoustical cues of group members in nocturnal mammals.     

Early growth-stages and classification of orthoceridan Cephalopods of the Darriwillian (Middle Ordovician) of Baltoscandia

Five apices of orthoceridan cephalopods from the early Middle Ordovician Holen Limestone of Öland, Sweden that where collected in the late 19th Century by G. Holm provide information on cephalopod evolution in the early Palaeozoic. The apices belong to specimens of the genus Hedstroemoceras Foerste, 1930 and Archigeisonoceras Chen, 1984. The apices are small in comparison with apices of other cephalopods of the Ordovician; the initial chambers of the shells of both genera are hemispherical and approximately 1 mm and 1.5 mm in cross-section diameter, respectively. The apical 2–3 mm of the shell are free from growth-lines and possess no cicatrix, though distinct longitudinal wrinkles are present. There is a slight variability of siphuncle position during early growth in Archigeisonoceras. It can be shown that the structure of the connecting ring of Hedstroemoceras is similar to that of other Orthocerida. Additionally, the hemispherical apex of Lituites perfectus Wahlenberg, 1821 gives evidence for the orthoceridan affinity of lituitidans. The investigation shows that early Middle Ordovician Orthocerida display a characteristic connecting ring structure, a characteristic apex morphology and variable siphuncular positions that differs significantly from other cephalopods of the Ordovician. Based on this evidence it is concluded that a small spherical apex is an autapomorphy of the Orthocerida. Moreover, this evidence supports a splitting of the order Orthocerida in two taxa of different affinities. The Orthocerida sensu stricto comprises orthocones with a tubular siphuncle nearly without endospiphuncular deposits, and a spherical apex. Embryonic shell, orthoceridan ancestry, orthoceridan classification.     

Intense ultrasonic clicks from echolocating toothed whales do not elicit anti-predator responses or debilitate the squid Loligo pealeii

Toothed whales use intense ultrasonic clicks to echolocate prey and it has been hypothesized that they also acoustically debilitate their prey with these intense sound pulses to facilitate capture. Cephalopods are an important food source for toothed whales, and there has probably been an evolutionary selection pressure on cephalopods to develop a mechanism for detecting and evading sound-emitting toothed whale predators. Ultrasonic detection has evolved in some insects to avoid echolocating bats, and it can be hypothesized that cephalopods might have evolved similar ultrasound detection as an anti-predation measure. We test this hypothesis in the squid Loligo pealeii in a playback experiment using intense echolocation clicks from two squid-eating toothed whale species. Twelve squid were exposed to clicks at two repetition rates (16 and 125 clicks per second) with received sound pressure levels of 199-226 dB re1 microPa (pp) mimicking the sound exposure from an echolocating toothed whale as it approaches and captures prey. We demonstrate that intense ultrasonic clicks do not elicit any detectable anti-predator behaviour in L. pealeii and that clicks with received levels up to 226 dB re1 microPa (pp) do not acoustically debilitate this cephalopod species.     

The ecological role of cephalopods and their representation in ecosystem models

Cephalopods, especially squids, are believed to have a structuring role in marine ecosystems as a link between different trophic levels, primarily due to their voracious prey consumption and high production rate. Cephalopod ecology, however, is still poorly understood as observational studies often give highly uncertain and variable results due to the peculiarities of cephalopod behaviour and biology, and their responsiveness to external drivers. This review evaluates our representation of cephalopods in ecosystem models and the insights given by these models on the role of cephalopods in our oceans. We examined ecosystem models from 13 regions to analyse the representation of cephalopods and compared their results to local trophic studies. Our analysis indicated that most ecosystem models inadequately include cephalopods in terms of model structure and parametrization; although some models still have the capacity to draw valuable conclusions regarding the impact and role of cephalopods within the system. Oceanic squid species have a major role linking trophic levels and food webs from different habitats. The importance of neritic species varies locally, but generally cephalopods have a substantial impact via their consumer role. To better understand the ecological role of cephalopods, improved representation of these species in ecosystem models is a critical requirement and could be achieved relatively easily to more accurately articulate the mechanisms regulating the ecological role of cephalopods.

     

Squid vascular endothelial growth factor receptor: a shared molecular signature in the convergent evolution of closed circulatory systems

SUMMARY The highly specialized cephalopod cardiovascular system has long been considered a valuable model for understanding the evolution of circulatory systems. Despite the number of studies devoted to this topic, the developmental regulatory mechanisms remain largely unexplored. Here, we focus on the vascular endothelial growth factor receptor (VEGFR). This factor is known to mediate levels of endothelial growth factor that is involved in hematopoiesis and vasculogenesis including multichambered heart development in vertebrates. We found a squid VEGFR ortholog that is expressed in the developing blood vessels, notably in the sheet-like endothelial cells of the systemic and branchial hearts. The highly restricted localization of VEGFR in the vascular endothelial cells and its shared expression pattern in the developing hearts of cephalopods and vertebrates suggest a shared molecular signature of closed circulatory systems that has been independently elaborated during evolution.     

The bearing of the new Late Cambrian monoplacophoran genus Knightoconus upon the origin of the Cephalopoda

Yochelson, E. L., Flower, R. H. & Webers, G. F.: The hearing of the new Late Cambrian monoplacophoran genus Knightoconus upon the origin of the Cephalopoda.
Knightoconus , a new genus of the Hypseloconidae (Mollusca: Monoplacophora) from rocks of early Franconian age in Antarctica, is multiseptate. The multiple septa are a criticàl feature to be expected in a form ancestral to cephalopods. Fossil cephalopods, however, invariably have a siphuncle as well as septa; some gastropods, some hyolithids, and some monoplacophorans also have septa but lack a siphuncle. Therefore, only the siphuncle can be considered a unique and particularly significant feature of the cephalopod shell. Hypothetical reconstructions of molluscan anatomy support the notion that cephalopods may have been derived directly from a hypseloconid having a high, slightly curved, multiseptate, bilaterally symmetrical shell, by the subsequent development of a siphuncle.     

A new baleen whale from the Late Miocene of Denmark and early mysticete hearing

Abstract:  The extinct mysticete fauna of the North East Atlantic is primarily known from the abundant but fragmented Belgian specimens. Compared to the well-preserved contemporary mysticete fauna from deposits in North America, there are only few near complete European Miocene mysticete fossils. Presented here is a new, almost complete fossil baleen whale Uranocetus gramensis gen. et sp. nov. from the Upper Miocene Gram Formation in South West Denmark. It is the first stem-balaenopterid that has an initial stage of reduction in the mandibular cavity and a rostral configuration that is intermediate between that of other stem-balaenopterids and true balaenopterids. It is likely that Uranocetus used a gulp feeding technique that approaches that of balaenopterids. Details of the periotic and mandibular morphology place Uranocetus in the family Diorocetidae Steeman 2007. The large mandibular cavity in Uranocetus and most other extinct mysticetes, when compared to the reduced condition in recent mysticetes, is not an indication that early mysticetes used odontocete-like echolocation. In Uranocetus and a distantly related mysticete, high frequency sounds in the range odontocetes use for echolocation would suffer a significant volume loss across the lateral mandibular wall on the passage towards the inner ear. A reduction in the mandibular cavity in separate evolutionary lineages of mysticetes may be the result of a shift towards the use of low frequency sounds.     

Stable isotopes, beaks and predators: a new tool to study the trophic ecology of cephalopods, including giant and colossal squids

Cephalopods play a key role in the marine environment but knowledge of their feeding habits is limited by lack of data. Here, we have developed a new tool to investigate their feeding ecology by combining the use of their predators as biological samplers together with measurements of the stable isotopic signature of their beaks. Cephalopod beaks are chitinous hard structures that resist digestion and the stable isotope ratios of carbon (delta13C) and nitrogen (delta15N) are indicators of the foraging areas and trophic levels of consumers, respectively. First, a comparison of delta13C and delta15N values of different tissues from the same individuals showed that beaks were slightly enriched in 13C but highly impoverished in 15N compared with lipid-free muscle tissues. Second, beaks from the same species showed a progressive increase in their delta15N values with increasing size, which is in agreement with a dietary shift from lower to higher trophic levels during cephalopod growth. In the same way, there was an increase in the delta15N signature of various parts of the same lower beaks in the order rostrum, lateral walls and wings, which reflects the progressive growth and chitinization of the beaks in parallel with dietary changes. Third, we investigated the trophic structure of a cephalopod community for the first time. Values of delta15N indicate that cephalopods living in slope waters of the subantarctic Kerguelen Islands (n=18 species) encompass almost three distinct trophic levels, with a continuum of two levels between crustacean- and fish-eaters and a distinct higher trophic level occupied by the colossal squid Mesonychoteuthis hamiltoni. delta13C values demonstrated that cephalopods grow in three different marine ecosystems, with 16 species living and developing in Kerguelen waters and two species migrating from either Antarctica (Slosarczykovia circumantarctica) or the subtropics (the giant squid Architeuthis dux). The stable isotopic signature of beaks accumulated in predators' stomachs therefore revealed new trophic relationships and migration patterns and is a powerful tool to investigate the role of the poorly known cephalopods in the marine environment.     

The cephalopod prey of the Weddell seal, <Emphasis Type="Italic">Leptonychotes weddellii</Emphasis>, a biological sampler of the Antarctic marine ecosystem

Weddell seals, Leptonychotes weddellii, are important apex predators in the food web of the Antarctic marine ecosystem. However, detailed information on their trophic relationships with cephalopods is scarce. Moreover, cephalopods play a key role in the marine environment, but knowledge of their feeding habits is limited by lack of data. Here, we have combined the use of this seal as a biological sampler together with measurements of the stable isotopic signature of the beaks of their cephalopod prey. Thus, the aims of the present study were: (1) to examine in detail the cephalopod portion of the diet of Weddell seals by means of scat analysis and (2) to assess the habitat use and trophic level of the different cephalopod prey taxa identified. From January to February 2009, a total of 48 faecal droppings were collected at Hope Bay, Antarctic Peninsula. Cephalopods were mainly represented by beaks (n = 83) which were identified to the lowest possible taxonomic level. Furthermore, subsamples of beaks were separated for further isotopic analysis. Relative abundance of stable isotopes of carbon (δ¹³C) and nitrogen (δ¹⁵N) was determined by continuous-flow isotope-ratio mass spectrometry. Cephalopods were represented uniquely by octopods of the subfamily Eledoninae. Pareledone turqueti was the dominant prey species followed by the papillated Pareledone species group and Adelieledone polymorpha. We conclude that Weddell seals preyed primarily on benthic prey resources. Furthermore, the relatively similar δ¹³C and δ¹⁵N values in beaks of the three octopod prey taxa suggest that these share the same type of habitat and occupy similar trophic level positions.