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This symposium presents different ecological and physiological strategies used by invertebrates to successfully adapt to aquatic environments. Adaptation has been studied mainly in adult animals, but the papers comprising the symposium emphasize ontogenetic strategies, starting from the principle that natural selection acts on all stages of development. Adaptive strategies may thus differ strikingly between developmental stages of the same organism. Invertebrates offer a wide array of ecophysiological models for study, and these are exemplified by the contributions to the symposium, which are briefly summarized. Future research in the field will 1, expand the number of models for comparative purposes; 2, examine the strategies, not only of larvae and juveniles, but also of embryos, eggs and reproductive cells; and 3, investigate the genetic basis of ontogenetic strategies.
The respiratory proteins hemoglobin and hemocyanin share the function of oxygen transport, but the proteins belong to separate gene families, and their active sites and the metal ions that bind the oxygen differ. Either hemoglobin or hemocyanin, but not both, is expressed in the hemolymph of many arthropod crustaceans. Hemoglobin is present in Branchiopoda, Ostracoda, Copepoda, rhizocephalan Cirripedia and one suborder of amphipodan Malacostraca, while hemocyanin has been described in Malacostraca. Recent work by several laboratories have provided new information on the gene structure, exon-intron patterns, site of synthesis and expression of hemoglobins in the branchiopods Artemia and Daphnia. These studies suggest the branchiopods are excellent model organisms for studies of oxygen sensors and hypoxia inducible transcription factors during developmental and adult stages. The focus in our laboratory on the ontogeny of hemocyanin in the Dungeness crab, Cancer magister, has demonstrated that both structure and function of hemocyanin change from megalopa to adult crab. The hemocyanin of an oceanic megalopa contains four subunits. Another subunit appears about the time of metamorphosis to first juvenile instar, and expression of a sixth subunit begins four or five molts later. The timing of onset of adult hemocyanin can be altered experimentally by food levels and temperature. Gene expression and functional properties of both red and blue oxygen transport proteins of crustaceans change during ontogeny to insure oxygen delivery appropriate for each developmental stage.
Patterns and mechanisms involved in the onset and development of cardiac function in a number of crustacean groups are critically reviewed. Irrespective of phylogeny, heart design and ecology, the onset of heart beat seems inextricably linked to the ontogeny of the thoracic segments where the heart is located. Initially the beat is erratic but soon becomes regular and the rate increases as development proceeds. However, still early in development the relationship between heart rate and body size shifts from a positive to a negative one. Nevertheless cardiac output continues to increase with increasing development, via increasing stroke volume. Some species in more ‘primitive’ groups develop and retain a myogenic heart beat. Others, with globular and tubular hearts, exhibit a shift from myogenicity to neurogenicity around the time the body size vs. heart rate relationship becomes negative. Very early cardiac function seems generally insensitive to external factors, such as temperature, oxygen and pollutants. Sensitivity to environmental factors increases with development, perhaps over the same timescale as the cardiac regulatory mechanisms appear.
Following a brief overview of the patterns of ontogeny of osmoregulation in postembryonic stages, this review concentrates on the ontogeny of osmoregulation during the embryonic development of crustaceans, particularly in those species living under variable or extreme salinity conditions and whose hatchlings osmoregulate at hatch. Two situations are considered, internal development of the embryos in closed incubating, brood or marsupial pouches, and external development in eggs exposed to the external medium. In both cases, embryos are osmoprotected from the external salinity level and variation, either by the female pouches or by the egg envelopes. The mechanisms of osmoprotection are discussed. During embryonic life, temporary or definitive osmoregulatory organs develop, with ion transporting cells and enzymes such as Na-K ATPase, permitting the embryos and then the hatchlings to osmoregulate and tolerate the external salinity.
We present an overview of the isolation and characterization of three hormones (or hormone families) important for the growth and development of decapod crustaceans. These hormones include the ecdysteroids (steroid molting hormones), the hyperglycemic hormone neuropeptide family, and the terpenoid methyl farnesoate. Using examples primarily from our laboratory, we describe work on these hormones using various life stages of the lobster (Homarus americanus) as the principal model.
Marine crustaceans present an extremely interesting set of examples in which to examine visual development and metamorphosis. Larvae of these animals are almost always planktonic, living in the light field of open waters. The presence of a simple, predictable photic environment, the relatively basic visual requirements of larvae, and the need to remain transparent to reduce predation lead to the use of a single eye type throughout all marine crustacean larvae. Adult crustaceans, on the other hand, use a greater diversity of optical designs than all other animals combined, occupy habitats from the deep sea to mountaintops, and have very complex visual systems and behaviors. Thus, visual development varies tremendously among modern Crustacea. In this brief review, we consider the structure and development of marine crustacean eyes, focusing on optics, retinal design, and metamorphosis of the visual pigments.
The early life cycle of brachyuran crabs has a planktonic dispersal stage consisting of a variable number of zoeal larvae followed by the molt to the megalopa stage. Megalopae undergo horizontal transport to the settlement site where they settle out of the water column and metamorphose to the first crab (juvenile) stage. This review provides an overview of recent laboratory studies of cues that shorten or lengthen the time to metamorphosis (TTM) of the megalopa stage. Megalopae cannot delay metamorphosis indefinitely and have a temporal threshold beyond which metamorphosis occurs without habitat cues. The TTM can be shortened about 15–25% upon exposure to acceleration cues, which include chemical cues and odors from adult substrate, aquatic vegetation, biofilms, conspecifics, estuarine water, humic acids, related crab species, and potential prey. Cues shown to delay metamorphosis include ammonium, hypoxia, predator odor and extreme temperature and salinity conditions. There is no evidence that structural mimics of natural substrate affect TTM.
Larvae from diverse marine-invertebrate phyla are able to respond rapidly to environmental cues to settlement and to undergo very rapid metamorphic morphogenesis because they share the developmental trait of metamorphic competence. The competent state, characteristic of larvae as diverse as those of cnidarian planulae, molluscan veligers, and barnacle cyprids, is one in which nearly all requisite juvenile characters are present in the larva prior to settlement. Thus metamorphosis, in response to more or less specific environmental cues (inducers), is mainly restricted to loss of larva-specific structures and physiological processes. Competent larvae of two “model marine invertebrates” studied in the authors' laboratory, the serpulid polychaete Hydroides elegans and the nudibranch Phestilla sibogae, complete metamorphosis in about 12 and 20 hr, respectively. Furthermore, little or no de novo gene action appears to be required during the metamorphic induction process in these species. Contrasting greatly with the slow, hormonally regulated metamorphic transitions of vertebrates and insects, competence and consequent rapid metamorphosis in marine invertebrate larvae are conjectured to have arisen in diverse phylogenetic clades because they allow larvae to continue to swim and feed in the planktonic realm while simultaneously permitting extremely fast morphological transition from larval locomotory and feeding modes to a different set of such modes that are adaptive to life on the sea bottom.
Vibration through the substrate has likely been important to animals as a channel of communication for millions of years, but our awareness of vibration as biologically relevant information has a history of only the last 30 yr. Morphologists know that the jaw mechanism of early amphibians allowed them to perceive vibration through the substrate as their large heads lay on the ground. Although the exact mechanism of vibration production and the precise nature of the wave produced are not always understood, recent technical advances have given answers to increasingly sophisticated questions about how animals send and receive signals through the substrate. Some of us have been forced to explore the use of vibration when all other attempts to manipulate animals in the field have failed, while others began to think about vibration to explain some of the puzzling behaviors of species they were studying in other contexts. It has thus become clear that the use of vibration in animal communication is much more widespread than previously thought. We now know that vibration provides information used in predator-prey interactions, recruitment to food, mate choice, intrasexual competition and maternal/brood social interactions in a range of animals from insects to elephants.
An amazing variety of mammals produce seismic vibrations by drumming a part of their body on a substrate. The drumming can communicate multiple messages to conspecifics about territorial ownership, competitive superiority, submission, readiness to mate, or presence of predators. Drumming also functions in interspecific communication when prey animals drum to communicate to predators that they are too alert for a successful ambush. The diversity of mammals that drum in varied contexts suggest independent evolution in different lineages. Footdrumming, as with other signals, probably originated by ritualization of older forms of behavior not associated with communication such as running and digging. Footdrumming patterns are species specific and range from single thumps to individual footdrum signatures. Although mammals communicate above ground with airborne drumming signals, they can also transmit sound seismically into the burrow where the signals become airborne and are received with ears especially adapted to hear low-frequency sound. Footdrumming has been studied the most extensively in kangaroo rats, Dipodomys. A comparison of species of different body mass shows that smaller sized, non-territorial species have no ritualized footdrumming; medium-sized species drum a simple pattern in limited contexts; while larger-sized species communicate territorial ownership with complex patterns. Future studies should examine the mechanics and energy requirements of drumming to test hypotheses about body size limitations on the evolution of footdrumming. Our understanding of drumming as communication is limited until investigators conduct field tests of responses to drumming signals in the contexts in which the signals are generated.
Bioseismic studies have previously documented the use of seismic stimuli as a method of communication in arthropods and small mammals. Seismic signals are used to communicate intraspecifically in many capacities such as mate finding, spacing, warning, resource assessing, and in group cohesion. Seismic signals are also used in interspecific mutualism and as a deterrent to predators. Although bioseismics is a significant mode of communication that is well documented for relatively small vertebrates, the potential for seismic communication has been all but ignored in large mammals. In this paper, we describe two modes of producing seismic waves with the potential for long distance transmission: 1) locomotion by animals causing percussion on the ground and 2) acoustic, seismic-evoking sounds that couple with the ground. We present recordings of several mammals, including lions, rhinoceroses, and elephants, showing that they generate similar acoustic and seismic vibrations. These large animals that produce high amplitude vocalizations are the most likely to produce seismic vibrations that propagate long distances. The elephant seems to be the most likely candidate to engage in long distance seismic communication due to its size and its high amplitude, low frequency, relatively monotonic vocalizations that propagate in the ground and have the potential to travel long distances. We review particular anatomical features of the elephant that would facilitate the detection of seismic waves. We also assess low frequency sounds in the environment such as thunder and the likelihood of seismic transmission. In addition, we present the potential role of seismic stimuli in human communication as well as the impact of modern anthropogenic effects on the seismic environment.
The subterranean environment is not favorable for the use of vision or the audition of airborne sounds as means of long-distance sensory perception. However, seismic vibrations have been shown to propagate at least an order of magnitude better than airborne sound between the burrow systems of the mole-rat Georychus capensis. The use of the seismic channel for communication underground is well documented for other species of bathyergids, as well as the spalacine mole-rat Nannospalax. It has recently been suggested that the golden mole Eremitalpa granti namibensis may also be sensitive to ground vibrations, in this case used in foraging in its desert habitat.
In this paper, the use of seismic signals among these and other fossorial mammals is reviewed from theoretical, behavioral and anatomical standpoints. The question of whether auditory or somatosensory means are used to detect vibratory signals is examined. Attempts to explain the distribution of seismic sensitivity and communication mechanisms among fossorial mammals are considered. The potential influences of different soil type and digging methods are discussed, and it is proposed that digging mechanisms involving the head might preadapt a fossorial mammal towards the development of seismic sensitivity.
Modern frogs and toads possess a structurally unique saccule, endowing them with seismic sensitivity greater than that observed so far in any other group of terrestrial vertebrates. In synchrony with their advertisement calls, approximately half of the calling males of one frog species, the Puerto-Rican white-lipped frog (Leptodactylus albilabris), produce impulsive seismic signals (thumps). The spectral distribution of power in these seismic signals matches precisely the spectral sensitivity of the frog's saccule. The signals have sufficient amplitude to be sensed easily by the frog's saccule up to several meters from the source—well beyond the typical spacing when these frogs are calling in a group. This circumstantial evidence suggests that white-lipped frogs may use the seismic channel in intraspecific communication, possibly as an alternative to the airborne channel, which often is cluttered with noise and interference. Using the frog's vocalizations as our assay, we set out to test that proposition. In response to playback calls, the male white-lipped frog adjusts several of its own calling parameters. The most conspicuous of these involves call timing—specifically the tendency for a gap in the distribution of call onsets, precisely timed with respect to the onsets of the playback calls. When the airborne component is unavailable (e.g., masked by noise), approximately one in five animals produces the calling gap in response to the seismic signals alone.
The male prairie mole cricket, Gryllotalpa major, native of the tallgrass prairie of the south central U.S., constructs a specialized acoustical burrow in the spring in the prairie soil from which he generates an airborne calling song that attracts flying females for mating. Males do not phonorespond to manipulations involving playbacks of airborne sounds. At the same time, vibrations with the same temporal scale and pattern as the airborne signal are produced in the substrate through an unknown mechanism. These ground vibrations can be distinguished from background vibrations in the soil at distances up to 3 m depending on soil conditions and conditions that control the background vibration environment (e.g., wind, highway traffic). We hypothesize that males use the vibration component of the call as information for spacing as they form display arenas, or leks. We used modified field recordings of soil vibrations from singing males with an electromechanical vibration exciter to simulate the vibration component of a calling song in playback experiments. Airborne sounds of males were monitored for two minutes before and two minutes after the introduction of the ground vibration stimulus with a tape recorder microphone placed 20 cm from the burrow opening. Males did respond to the manipulation experiment; although, we observed individual variation in the level of response.
Communication among members of a colony is a key feature of the success of eusocial insects. The same may be true in other forms of insect sociality. I suggest that substrate-borne vibrational communication is important in the success of group-living, herbivorous insects. I examine three challenges encountered by herbivorous insects: locating and remaining in a group of conspecifics; locating food resources; and avoiding predation. Studies of groups of immature treehoppers, sawflies and butterflies suggest that vibrational communication can be important in each of these contexts, enhancing the ability of these group-living herbivores to exploit the resources of their host plants.
Male Graminella nigrifrons participate in alternating choruses. Vibrational calls emitted by males consist of three sections (S1, S2, and S3) that differ in pattern of amplitude modulation. In this study we examined the response of single males to synthetic choruses and to isolated call components to gain insight into the regulation of chorus structure. Males initiated calls primarily during the silent periods within synthetic choruses. In all 15 trials the number of overlapping calls and the duration of overlap was significantly less than expected if males call at random. Playback of S2, S3, or random noise while males emitted S1 caused males to interrupt calling, whereas males continued to call when S1 or no signal was played. In a related experiment, we played S2 or no signal while males were beginning to emit the S1, S2, or S3 phase of their calls. In response to this playback the duration of S1 and S3 was reduced, but the duration of S2 was not affected. These results suggest that an inhibitory-resetting mechanism may result in alternation of calls in this leafhopper.
As burrowing, nocturnal predators of small arthropods, sand scorpions have evolved exquisite sensitivity to vibrational information that comes to them through the substrate they live on, dry sand. Over distances of a few decimeters, sand conducts low velocity (∼50 m/sec) surface (Rayleigh) waves of sufficient amplitude and bandwidth (200<f<500 Hz) to be biologically detectable. Eight acceleration-sensitive receptors (slit sensilla) at the tips of the scorpion's circularly arranged legs detect surface waves generated by prey movements or “juddering” signals from other scorpions. From this input alone, direction of the disturbance source is calculated up to 20 cm distance. By ablating slit sensilla in various combinations on the eight legs, the contribution each makes in computing target location can be assessed. Other behavioral experiments show that differential timing of surface wave arrival at each sensor is most likely the cue that determines target location. Given the simplicity of this sensory system, a computational theory to account for wave source localization has been developed using a population of second-order neurons, each receiving excitatory input from one vibration receptor and inhibition from the triad of receptors opposite to it in the eight-element array. Input from a passing surface wave opens and closes a time widow, the width of which determines the firing probability of second-order neurons. Target direction is encoded as the relative excitation of these neurons, and stochastic optimization tunes the relative strengths of excitatory and inhibitory inputs for accuracy of response. The excellent agreement between predictions of the model and observed behavior of sand scorpions confirms a simple theory for computational mapping of surface vibration space.
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