Physiological mechanisms in the control of bioluminescent countershading in a midwater shrimp

In the oceanic midwater environment, most animals have evolved an extraordinary anti‐predation behavior using bioluminescent countershading (counterillumination) to help them remain cryptic to visual predators. For the midwater penaeid shrimp, Sergestes similis, the interaction of both hormonal and neural systems may be involved in the control of counterillumination. S. similis responds to downward‐directed illumination, detected by the eyes, with light emission from five hepatic light organs. Dark‐adapted specimens undergo a slow induction process prior to production of the conventional counterillumination response. The induction of bio‐luminescence may involve a hormonal pathway mediated by the light‐adapting retinal distal pigment dispersing hormone. Once induced, the rapid control of counterillumination may involve a neural pathway. Because counterilluminating animals directly respond to their optical environment, an understanding of the control of bioluminescence provides an insight into the poorly understood visual processing capabilities of deep‐sea animals.     

Evolution of the light organ system in ponyfishes (Teleostei: Leiognathidae)

Members of the leiognathid subfamily Gazzinae, comprising approximately two‐thirds of ponyfish species, are sexually dimorphic with regard to features of the light organ system (LOS). In Gazzinae, the circumesophageal light organ (LO) of males is enlarged and varies in shape compared with similarly sized conspecific females. In association with male species‐specific translucent external patches on the head and flank, these sexually dimorphic LO features are hypothesized to be correlated with species‐specific luminescence displays. Anatomical differences in LO shape, volume, and orientation, and its association with the gas bladder and other internal structures that function in light emission, are compared to observations of luminescence displays for every major lineage within Leiognathidae. We reconstruct the character evolution of both internal and external morphological features of the LOS to investigate the evolution of LO sexual dimorphism and morphology. Both internal and external sexual dimorphism in the ponyfish LOs were recovered as most likely to have evolved in the common ancestor of Leiognathidae, and likelihood‐based correlation analyses indicate that the evolution of internal and external dimorphism in males is statistically correlated. Magnetic resonance imaging technology was applied to examine the unique internal LOs of ponyfishes in situ, which provides a new metric (LO index) for comparison of LO structure across lineages. J. Morphol. 2011. © 2011 Wiley‐Liss, Inc.     

Phylogeography and support vector machine classification of colour variation in panther chameleons

Lizards and snakes exhibit colour variation of adaptive value for thermoregulation, camouflage, predator avoidance, sexual selection and speciation. Furcifer pardalis, the panther chameleon, is one of the most spectacular reptilian endemic species in Madagascar, with pronounced sexual dimorphism and exceptionally large intraspecific variation in male coloration. We perform here an integrative analysis of molecular phylogeography and colour variation after collecting high‐resolution colour photographs and blood samples from 324 F. pardalis individuals in locations spanning the whole species distribution. First, mitochondrial and nuclear DNA sequence analyses uncover strong genetic structure among geographically restricted haplogroups, revealing limited gene flow among populations. Bayesian coalescent modelling suggests that most of the mitochondrial haplogroups could be considered as separate species. Second, using a supervised multiclass support vector machine approach on five anatomical components, we identify patterns in 3D colour space that efficiently predict assignment of male individuals to mitochondrial haplogroups. We converted the results of this analysis into a simple visual classification key that can assist trade managers to avoid local population overharvesting.     

Vision in the deep sea

The deep sea is the largest habitat on earth. Its three great faunal environments--the twilight mesopelagic zone, the dark bathypelagic zone and the vast flat expanses of the benthic habitat--are home to a rich fauna of vertebrates and invertebrates. In the mesopelagic zone (150-1000 m), the down-welling daylight creates an extended scene that becomes increasingly dimmer and bluer with depth. The available daylight also originates increasingly from vertically above, and bioluminescent point-source flashes, well contrasted against the dim background daylight, become increasingly visible. In the bathypelagic zone below 1000 m no daylight remains, and the scene becomes entirely dominated by point-like bioluminescence. This changing nature of visual scenes with depth--from extended source to point source--has had a profound effect on the designs of deep-sea eyes, both optically and neurally, a fact that until recently was not fully appreciated. Recent measurements of the sensitivity and spatial resolution of deep-sea eyes--particularly from the camera eyes of fishes and cephalopods and the compound eyes of crustaceans--reveal that ocular designs are well matched to the nature of the visual scene at any given depth. This match between eye design and visual scene is the subject of this review. The greatest variation in eye design is found in the mesopelagic zone, where dim down-welling daylight and bio-luminescent point sources may be visible simultaneously. Some mesopelagic eyes rely on spatial and temporal summation to increase sensitivity to a dim extended scene, while others sacrifice this sensitivity to localise pinpoints of bright bioluminescence. Yet other eyes have retinal regions separately specialised for each type of light. In the bathypelagic zone, eyes generally get smaller and therefore less sensitive to point sources with increasing depth. In fishes, this insensitivity, combined with surprisingly high spatial resolution, is very well adapted to the detection and localisation of point-source bioluminescence at ecologically meaningful distances. At all depths, the eyes of animals active on and over the nutrient-rich sea floor are generally larger than the eyes of pelagic species. In fishes, the retinal ganglion cells are also frequently arranged in a horizontal visual streak, an adaptation for viewing the wide flat horizon of the sea floor, and all animals living there. These and many other aspects of light and vision in the deep sea are reviewed in support of the following conclusion: it is not only the intensity of light at different depths, but also its distribution in space, which has been a major force in the evolution of deep-sea vision.     

Sound or Silence: Call Recognition in the Temporal Domain by the Frog Allobates femoralis

Acoustic communication often mediates agonistic interactions in territorial species. Because both the reaction to potential intruders and the lack thereof are costly, mechanisms that allow recognition of conspecific signals should be evident in intrasexual communication systems. While the spectral domain of the recognition space of the frog Allobates femoralis appears asymmetrically shaped in a way that reduces masking interference by the often syntopic frog Ameerega trivittata, frequency alone does not appear to account for the correct identification of conspecific intruders (Amézquita et al., Animal Behaviour, 70, 2005: 1377). As signal recognition may rely on a combination of spectral and temporal parameters of the signal, we test here the subsequent prediction that the recognition space should be asymmetrical in the temporal domain as well. We conducted playback experiments with 80 synthetic calls on 30 males and modeled all‐or‐none responses to define unidimensional functions of the recognition space for two call parameters: note duration and internote interval. For both parameters, male maximal response matched very well the average values of the conspecific signal and decreased with concomitant deviations from these values. While the response curves exceeded the range of signal variation and were not asymmetrical for either call parameter, they differed in breadth. The highest male permissiveness to variation in internote interval, as evidenced by a broader response curve, coincided with the lower probability of between‐species overlap in this signal parameter. Together with previous studies, our data suggest that a combination of spectral and temporal parameters of the advertisement call is necessary for recognition of calling intruders in A. femoralis. Our results emphasize the importance of multidimensional approaches in understanding signal recognition mechanisms in acoustically complex environments.     

Mate Choice by Both Sexes Maintains Reproductive Isolation in a Species Flock of Pupfish (Cyprinodon spp) in the Bahamas

Female and male mate choices can reinforce reproductive isolation after sympatric speciation. Using a binary choice design, we examine the importance of visual cues in female mate choice in all three sympatric species of pupfish on San Salvador Island. We also examine the importance of olfactory cues in female choice of the hard‐shelled invertebrate specialist (Cyprinodon brontotheroides). We examine male mate choice in two of the three species, the scale eater (C. desquamator) and the detritivore (C. variegatus). Females of all three species use visual cues and prefer conspecific males. C. brontotheroides females do not use olfactory cues to discriminate between conspecific and heterospecific males. Males of C. desquamator and C. variegatus also preferentially court conspecific females. Thus, mutual mate choice, where both females and males exhibit mate choice, acts as a strong behavioral pre‐mating isolation mechanism in these sympatrically speciated pupfish.     

Length–weight relationships of 11 deep‐sea fishes from the western Bay of Bengal and Andaman waters,India

Length–weight relationships (LWRs) are presented for 11 deep‐sea fishes caught in the western Bay of Bengal and Andaman waters during August 2010 using a 38 m high speed demersal trawl II (HSDT II, crustacean version, codend mesh size 40 mm) and a 45.6 m Expo model demersal trawl (codend mesh size 30 mm). The b values ranged from 2.34 to 3.3 and the coefficient of variation (r²) ranged from .82 to .98. LWR estimates of eight deep‐sea fishes are provided for the first time. The estimated LWR values were compared with the Bayesian LWR estimates available in FishBase, based on models developed to improve the accuracy and predictability of species‐specific growth parameters of data‐poor species.     

Unexpected diversity of bioluminescence in planktonic worms

The vast majority of pelagic bioluminescent organisms emit a blue light with emission maxima (λ_max) ranging from 450 to 490 nm. Among the known outliers, the tomopterids (Annelida: Polychaeta) are usually described as yellow‐emitters (λ_max = 565–570 nm) for which bioluminescence functions as a specific recognition signal. Here, we report the first data regarding the colours emitted by four different tomopterid species, Tomopteris pacifica, T. carpenteri, T. septentrionalis and T. planktonis. Surprisingly, T. planktonis is a blue‐emitter (λ_max = 450 nm). Our pharmacological results on T. planktonis support cholinergic control, as recently demonstrated in the yellow‐emitter, T. helgolandica. Moreover, as revealed by epifluorescence microscopy, the light seems to be produced in both species from the same yellow‐pigmented parapodial glands. Despite these similarities, tomopterids express an unexpected diversity of bioluminescent colour patterns. This leads us to reassess the ecological value of bioluminescence within this group.     

Associational effects and the maintenance of polymorphism in plant defense against herbivores: review and evidence

Many plant species have evolved defense traits against herbivores. Associational effects (AEs) refer to a kind of apparent interaction where the herbivory risk to a focal plant species depends on the composition of other plant species in a neighborhood. Despite ample evidence for AEs between different plant species, this point of view has rarely been applied to polymorphism in defense traits within a plant species. The purpose of this review is to highlight an overlooked role of conspecific AEs in maintaining polymorphism in antiherbivore defense. First, I present a general review of AE between plant species and its role in the coexistence of plant species. This viewpoint of AE can be applied to genetic polymorphism within a plant species, as it causes frequency‐ and density‐dependent herbivory between multiple plant types. Second, I introduce a case study of conspecific AEs in the trichome‐producing (hairy) and glabrous plants of Arabidopsis halleri subsp. gemmifera. Laboratory and semi‐field experiments illustrated that AEs against the brassica leaf beetle Phaedon brassicae mediate a minority advantage in defense and fitness between hairy and glabrous plants. Combined with a statistical modeling approach, field observation revealed that conspecific AEs can maintain the trichome dimorphism via negative frequency‐dependent selection in a plant population. Finally, I discuss spatial and temporal scales at which AEs contribute to shaping genetic variation in antiherbivore defense in a plant metapopulation. Based on the review and evidence, I suggest that AEs play a key role in the maintenance of genetic variation within a plant species.     

Spatial and temporal patterns of genetic variation in the widespread antitropical deep‐sea coral Paragorgia arborea

Numerous deep‐sea species have apparent widespread and discontinuous distributions. Many of these are important foundation species, structuring hard‐bottom benthic ecosystems. Theoretically, differences in the genetic composition of their populations vary geographically and with depth. Previous studies have examined the genetic diversity of some of these taxa in a regional context, suggesting that genetic differentiation does not occur at scales of discrete features such as seamounts or canyons, but at larger scales (e.g. ocean basins). However, to date, few studies have evaluated such diversity throughout the known distribution of a putative deep‐sea species. We utilized sequences from seven mitochondrial gene regions and nuclear genetic variants of the deep‐sea coral Paragorgia arborea in a phylogeographic context to examine the global patterns of genetic variation and their possible correlation with the spatial variables of geographic position and depth. We also examined the compatibility of this morphospecies with the genealogical‐phylospecies concept by examining specimens collected worldwide. We show that the morphospecies P. arborea can be defined as a genealogical‐phylospecies, in contrast to the hypothesis that P. arborea represents a cryptic species complex. Genetic variation is correlated with geographic location at the basin‐scale level, but not with depth. Additionally, we present a phylogeographic hypothesis in which P. arborea originates from the North Pacific, followed by colonization of the Southern Hemisphere prior to migration to the North Atlantic. This hypothesis is consistent with the latest ocean circulation model for the Miocene.     

DARK ADAPTATION AND VISUAL SENSITIVITY IN SHALLOW AND DEEP-DIVING PINNIPEDS1

Pinnipeds forage almost exclusively underwater. Consequently, observing them is difficult and relatively little is known of how they use their senses to locate prey, avoid predators, and navigate while diving. Vision has been presumed to be of primary importance, although previous measurements of visual functioning in pinnipeds have been restricted to just a few shallow-diving species. As diving pinnipeds experience rapid changes in light levels during descent/ascent and low light levels at depth, it has not been clear whether they possess visual capabilities adequate for use while diving, particularly in the case of deep-diving species. To examine this issue, behavioral psychophysics have been used to assess and compare the dark adaptation rates and relative light sensitivities of a deep-diving pinniped (northern elephant seal, Mirounga angustirostris), two shallow-diving species (California sea lion, Zalophus californianus, and harbor seal, Phoca vitulina), and a human subject. In comparison to the human subject, both the California sea lion and the harbor seal dark-adapted relatively quickly and were more light sensitive. These findings suggest that both of these species are well suited for vision in the moderately dim shallow-water environments in which they dive to forage. In contrast, the elephant seal reached complete dark adaptation in less than half the time taken by the other pinnipeds, and it was significantly more light sensitive. Unlike the shallower-diving species, the visual abilities of the elephant seal are commensurate with the extreme conditions experienced while deep diving. Thus, we conclude that elephant seals are sufficiently adapted to rely on vision underwater, even while diving to depths in excess of 1000 meters where bioluminescence may be the sole source of ambient light.     

Heterospecific female mimicry in Ficedula flycatchers

Mimicry is a widespread phenomenon. Vertebrate visual mimicry often operates in an intraspecific sexual context, with some males resembling conspecific females. Pied flycatcher (Ficedula hypoleuca) dorsal plumage varies from the ancestral black to female‐like brown. Experimental studies have shown that conspecific and heterospecific (collared flycatcher, F. albicollis) individuals of both sexes respond, at least initially, to brown individuals as if they were female. We quantified the perceptual and biochemical differences between brown feathers and found that brown pied flycatcher males are indistinguishable from heterospecific, but not from conspecific, females in both aspects. To our knowledge, this is the first evidence of a visual mimetic signalling system in a sexual context where the model is heterospecific to the mimic. By only mimicking heterospecific females, brown pied flycatcher males can establish territories next to the more dominant collared flycatcher in sympatry, suffer less aggression by darker conspecifics in allopatry and preserve within‐species sexual recognition throughout the breeding range. A closer look at the evolutionary history and ecology of these two species illustrates how such a mimetic system can evolve. Although likely rare, this phenomenon might not be unique to Ficedula flycatchers.     

Sex determination of the Early Cretaceous clam shrimp Eosestheria middendorfii (Yixian Formation,China)

Clam shrimps have been recognized as a key group for the study of reproductive system evolution, owing to the diversity of sexual systems in extant members. However, there are comparatively little data on fossil taxa. In this study, we reveal the sexual system of the Early Cretaceous clam shrimp Eosestheria middendorfii (Yixian Formation, China). This is the first study that restricts the analysis to a single cohort, minimizing the otherwise considerable impact of ecophenotypic variation within this species. In addition, the presence of egg clutches, which identifies some individuals as either female or hermaphroditic, serves as an independent indicator for sex prior to the statistical treatment of the data. Obligate sexuality (‘dioecy’) is the inferred reproductive system for E. middendorfii and sexual dimorphism accounts for about 10% of the adult shape variation. Carapace shape variation resulting from malformation and deformation is more pronounced than the underlying sexual dimorphism. Subtle sexual dimorphism, smaller and slightly more elongate females, lateral egg clutches, and egg diameters of about 140 μm indicate that E. middendorfii is closely allied with the extant family Cyzicidae.     

Net‐spinning caddisfly distribution in large regulated rivers

1. Most of the world's large rivers are dammed for the purposes of water storage, flood control, and power production. Damming rivers fundamentally alters water temperature and flows in tailwater ecosystems, which in turn affects the presence and abundance of downstream biota.
2. We collaborated with more than 200 citizen scientists to collect 2,194 light trap samples across 2 years and more than 2,000 river km. Samples contained 16,222 net‐spinning caddisfly (Hydropsyche) individuals across six species. We used these data to model the distribution of Hydropsyche throughout the Colorado River Basin in the western U.S.A. to identify the roles of water temperature, flows, and species‐specific morphology in determining aquatic species distributions throughout a large arid watershed that has been heavily altered by damming.
3. We predicted that water temperatures would determine Hydropsyche presence and abundance to a greater extent than diel variation in river stage associated with hydropower production. Among many species, adult female Hydropsychids are morphologically adapted to swim to deep‐water oviposition sites. We predicted that the presence of this ability would negate the otherwise deleterious effects of high stage change on caddisfly egg mortality.
4. We found that distributions of the two most widespread species, Hydropsyche occidentalis and Hydropsyche oslari (92% of total Hydropsyche captured), were both predicted by water temperatures. However, we also found that the abundance of H. oslari decreased by as much as 10‐fold as diel stage change increased, despite the presence of female morphological adaptations for deep‐water oviposition. We found sexual dimorphism and evidence for deep‐water swimming adaptations in 5/6 species.
5. Our results show that net‐spinning caddisflies have species‐specific responses to environmental variation and suggest that environmental flows designed to reduce diel stage change and destabilise water temperatures may improve habitat quality for these ubiquitous and important aquatic insects.

     

Intraspecific variation in the skull morphology of the black caiman Melanosuchus niger (Alligatoridae,Caimaninae)

Melanosuchus niger is a caimanine alligatorid widely distributed in the northern region of South America. This species has been the focus of several ecological, genetic and morphological studies. However, morphological studies have generally been limited to examination of interspecific variation among extant species of South American crocodylians. Here, we present the first study of intraspecific variation in the skull of M. niger using a two‐dimensional geometric morphometric approach. The crania of 52 sexed individuals varying in size were analysed to quantify shape variation and to assign observed shape changes to different types of intraspecific variation, that is, ontogenetic variation and sexual dimorphism. Most of the variation in this species is ontogenetic variation in snout length, skull depth, orbit size and the width of the postorbital region. These changes are correlated with bite force performance and probably dietary changes. However, a comparison with previous functional studies reveals that functional adaptations during ontogeny seem to be primarily restricted to the postrostral region, whereas rostral shape changes are more related to dietary shifts. Furthermore, the skulls of M. niger exhibit a sexual dimorphism, which is primarily size‐related. The presence of non‐size‐related sexual dimorphism has to be tested in future examinations.     

Invertebrate population genetics across Earth's largest habitat: The deep‐sea floor

Despite the deep sea being the largest habitat on Earth, there are just 77 population genetic studies of invertebrates (115 species) inhabiting non‐chemosynthetic ecosystems on the deep‐sea floor (below 200 m depth). We review and synthesize the results of these papers. Studies reveal levels of genetic diversity comparable to shallow‐water species. Generally, populations at similar depths were well connected over 100s–1,000s km, but studies that sampled across depth ranges reveal population structure at much smaller scales (100s–1,000s m) consistent with isolation by adaptation across environmental gradients, or the existence of physical barriers to connectivity with depth. Few studies were ocean‐wide (under 4%), and 48% were Atlantic‐focused. There is strong emphasis on megafauna and commercial species with research into meiofauna, “ecosystem engineers” and other ecologically important species lacking. Only nine papers account for ~50% of the planet's surface (depths below 3,500 m). Just two species were studied below 5,000 m, a quarter of Earth's seafloor. Most studies used single‐locus mitochondrial genes revealing a common pattern of non‐neutrality, consistent with demographic instability or selective sweeps; similar to deep‐sea hydrothermal vent fauna. The absence of a clear difference between vent and non‐vent could signify that demographic instability is common in the deep sea, or that selective sweeps render single‐locus mitochondrial studies demographically uninformative. The number of population genetics studies to date is miniscule in relation to the size of the deep sea. The paucity of studies constrains meta‐analyses where broad inferences about deep‐sea ecology could be made.     

Sexual dimorphism and allometry in two seed beetles (Coleoptera: Bruchidae)

Male Callosobruchus chinensis (Coleoptera: Bruchidae) have elaborated, pectinate antennae, which are absent from conspecific females and both sexes of a congener, Callosobruchus maculatus. To begin to unravel the mechanisms producing this striking dimorphism, we examined which morphological traits best explain body size variation in bruchid beetles and quantified sexual dimorphism of antenna size through allometric analyses. Using principal component analyses, we found that elytron length and pronotum width were significantly correlated with the first principal component, which was interpreted as explaining variation in body size. Regressions of log‐transformed body size measures on log‐transformed antenna length revealed that males of both species had longer antennae than conspecific females for any given body size, although most of this effect was attributable to higher intercepts, rather than increased allometry, in males. Comparisons among heterospecific males revealed that C. maculatus males have noticeably longer antennae than C. chinensis males at large body sizes. Callosobruchus chinensis males, thus, appear to have increased the receptive area of their antennae by adding to the width of, rather than further elongating, their antennae. Finally, we found evidence for positive allometry between log‐transformed antenna length and log‐transformed antenna width in C. chinensis males. We discuss our results in the context of evidence supporting the presence of an additional, and potentially unique, sex pheromone in C. chinensis females.     

Species recognition in Darwin's finches (Geospiza, Gould). III. Male responses to playback of different song types,dialects and heterospecific songs

The songs of the six different species of Darwin's ground finches (Geospiza) on the Galápagos Islands are difficult to distinguish unambiguously because of high levels of intraspecific variation and interspecific similarity in some cases. We recorded the responses of males on five islands to playback of (a) the two main conspecific song types, A and B, (b) local conspecific and heterospecific song, and (c) local and foreign dialects. Males reacted equally strongly to different conspecific song types (A and B), but responded significantly more strongly to local conspecific song than to either heterospecific song or foreign dialect. These results are inconsistent with earlier suggestions that song types subdivide Geospiza populations and that Geospiza song lacks species-distinctness because of loss-of-contrast or character convergence. The apparent paradox of low song specificity and well-developed acoustic discrimination is discussed in the light of other data showing that close-range species recognition also depends on visual cues.     

Sex Differences in Mate Preference Between Two Hybridizing Species of Poeciliid Fish

When hybridization between two species in secondary contact is costly, natural selection should favor pre‐mating isolation barriers. The invasive Gambusia affinis has been introduced to habitats of a closely related species, the endangered Gambusia nobilis. Although other Gambusia species readily hybridize in secondary contact, previous studies in this system found low abundance of hybrids in sympatry. To examine whether hybridization is limited by behavioral pre‐mating isolation that may have evolved in allopatry, I examined each species’ mating preferences using individuals from allopatric populations in male and female visual/olfactory association preference tests as well as open mating tests with and without male–male competition. Gambusia affinis and G. nobilis males had significant association preference for conspecific females in visual/olfactory tests. Only G. nobilis females had statistically significant preference for conspecific males. In open mating tests, males of both species had lower chase times overall when in competition, but there was no difference in number of copulation attempts. Males of both species had higher copulatory success rates with conspecific females when in competition, suggesting females may exert some control over copulation success of males. These results suggest that there are differences in mating preferences between these species. This mate choice may act as a pre‐mating isolating barrier to reduce hybridization in sympatry, a proposed threat to the endangered G. nobilis.