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Both plant biologists and animal biologists seek to understand how their focal organisms have evolved to interact with the environment. Despite this similarity in goals, the differing biology of plants and animals as well as other factors have led these scientific communities to diverge. Scientific discoveries that have occurred in each community in relative isolation may advance progress in the other community and set the stage for broad scientific syntheses. The accompanying papers, summarized herein, exemplify such discoveries, and collectively argue that the plant and animal ecophysiological communities have much to gain from improved cooperation and communication.
Both plants and animals respond to stress by using adaptations that help them evade, tolerate, or recover from stress. In a synthetic paper A. D. Bradshaw (1972) noted that basic biological differences between plants and animals will have diverse evolutionary consequences, including those influencing how they deal with stress. For instance, Bradshaw argued that animals, because they have relatively well-developed sensory and locomotor capacities, can often use behavior and movement to evade or ameliorate environmental stresses. In contrast, he predicted that plants will have to emphasize increased physiological tolerance or phenotypic plasticity, and also that plants should suffer stronger selection and show more marked differentiation along environmental gradients. Here we briefly review the importance of behavior in mitigating stress, the behavioral capacities of animals and plants, and examples of plant responses that are functionally similar to behaviors of animals. Next, we try to test some of Bradshaw's predictions. Unfortunately, critical data often proved non-comparable: plant and animal biologists often study different stressors (e.g., water versus heat) and measure different traits (photosynthesis versus locomotion). Nevertheless, we were able to test some of Bradshaw's predictions and some related ones of our own. As Bradshaw predicted, the phenology of plants is more responsive to climate shifts than is that of animals and the micro-distributions of non-mobile, intertidal invertebrates (“plant” equivalents) are more sensitive to temperature than are those of mobile invertebrates. However, mortality selection is actually weaker for plants than for animals. We hope that our review not only redraws attention to some fascinating issues Bradshaw raised, but also encourages additional tests of his predictions. Such tests should be informative.
Plants respond to changes in atmospheric carbon dioxide. To herbivores, the decreased leaf protein contents and increased C/N ratios common to all leaves under elevated atmospheric carbon dioxide imply a reduction in food quality. In addition to these fine-scale adjustments, the abundance of C3 and C4 plants (particularly grasses) are affected by atmospheric carbon dioxide. C4 grasses currently predominate over C3 grasses in warmer climates and their distributions expand as atmospheric carbon dioxide levels decreased during glacial periods. C4 grasses are a less nutritious food resource than C3 grasses both in terms of reduced protein content and increased C/N ratios. There is an indication that as C4-dominated ecosystems expanded 6–8 Ma b.p., there were significant species-level changes in mammalian grazers. Today there is evidence that mammalian herbivores differ in their preference for C3versus C4 food resources, although the factors contributing to these patterns are not clear. Elevated carbon dioxide levels will likely alter food quality to grazers both in terms of fine-scale (protein content, C/N ratio) and coarse-scale (C3versus C4) changes.
We explore in this paper how animals can be affected by variation in climate, topography, vegetation characteristics, and body size. We utilize new spatially explicit state-of-the-art models that incorporate principles from heat and mass transfer engineering, physiology, morphology, and behavior that have been modified to provide spatially explicit hypotheses using GIS. We demonstrate how temporal and spatial changes in microclimate resulting from differences in topography and vegetation cover alter animal energetics, and behavior. We explore the impacts of these energetic predictions on elk energetics in burned and unburned stands of conifer in winter in Yellowstone National Park, chuckwalla lizard distribution limits in North America, California Beechey Ground squirrel and Dusky Footed woodrat mass and energy requirements and activity patterns on the landscape, their predator prey interactions with a rattlesnake, Crotalus viridis, and shifts in that food web structure due to topographic and vegetative variation. We illustrate how different scales of data/observation provide different pieces of information that may collectively define the real distributions of a species. We then use sensitivity analyses of energetic models to evaluate hypotheses about the effects of changes in core temperature (fever) global climate (increased air temperature under a global warming scenario) and vegetation cover (deforestation) on winter survival of elk, the geographic distribution of chuckwallas and the activity overlap of predator and prey species within a subset of commonly observed species in a terrestrial food web. Variation in slope and aspect affect the spatial variance in solar radiation incident on the ground, hence ground surface temperature, at the same elevation, same hourly 2 m air temperatures, and wind speeds. We illustrate visually how spatial effects and landscape heterogeneity make statistical descriptions of animal responses problematic, since multiple distributions of their responses to climate, topography, and vegetation on the landscape can yield the same descriptive statistics, especially at high (30 m) resolution. This preliminary analysis suggests that the model has far-reaching implications for hypothesis testing in ecology at a variety of spatial and temporal scales.
Until recently, the study and understanding of plant and animal signalling and response mechanisms have developed independently. Recent biochemical and molecular work is producing a growing list of elements involved in responses to biotic and abiotic stimuli that are very similar across kingdoms. Some of the more interesting examples of these include prostaglandin/octadecanoid-mediated responses to wounding, steroid-based signalling systems, and pathogen-recognition mechanisms. Some of these similarities probably represent evolutionary convergence; others may be ancestral to plants and animals. Ecological and evolutionary implications of such overlaps include the existence of pathogens that can cause disease in plants and animals, the ability of herbivores to manipulate plant responses, usurpation of microbial mechanisms and genes by herbivorous animals and plants, evolution of plant defenses exploiting shared signals in animals, and the medicinal use of plants by humans. Comparative study of the signalling and response mechanisms used by plants, animals, and microbes provides novel and useful insights to the ecology and evolution of interactions across kingdoms.
In order to adapt to low oxygen it is necessary first to be able to detect hypoxia, then to initiate the appropriate defense mechanisms. There are two basic detectors: molecular sensors that are directly linked to gene regulation and metabolic indicators that are triggered when the cell goes into a state of energy imbalance. The molecular responses to oxygen deprivation are characterized in a variety of cell types and include activation of oxygen sensors, signaling through specific promoter elements and subsequent downstream adaptations. Many of the components are highly conserved across species. In the brain, the most hypoxic vulnerable of all vertebrate tissues, low oxygen quickly results in a fall in ATP and a consequent increase in adenosine. Both changes act as metabolic indicators of cellular energy crisis and effect mechanisms to reduce metabolic demand. Important lessons on the potential scope of such mechanisms can be provided by the anoxic tolerant turtle brain. Anoxia provokes an early release of adenosine which mediates channel arrest, causes a reduction in K efflux and Ca2 influx, and inhibits excitatory neurotransmitter release. There is a differential expression between normoxic and anoxic turtle brains of transcripts encoding the immediate early gene products c-fos and c-jun, the HSP-70 and the apoptosis regulators bcl-2 and bax.
Because of anthropogenic increases in atmospheric CO2 content, there is a need to understand how organisms sense and respond to CO2 variation. An important distinction is whether CO2 responses result from direct effects of CO2 on signal-transduction pathways, enzyme catalysis, or regulatory processes, as opposed to indirect, secondary responses that are a consequence of the direct effects. In plants, direct effects occur because rising CO2 A) increases the activity of Ribulose-1,5-bisphopshate carboxylase/oxygenase (Rubisco) via its role as a substrate for RuBP carboxylation and its inhibition of RuBP oxygenation; B) reduces stomatal aperture; C) alters mitochondrial respiration; and D) possibly reduces transcription of genes for Rubisco activase and carbonic anhydrase. Because of these direct effects, the carbon and water balance of plants is altered leading to secondary effects on growth, resource partitioning and defense compound synthesis. Reduced investment in photosynthetic protein is one of the characteristic acclimation responses of plants to high CO2. This is modulated by increased carbohydrate levels, probably in concert with hormone signals from the roots. Roots are hypothesized to be the main control points for CO2 acclimation because they are well situated to integrate the carbohydrate status of the plant. In higher fungi, development of the mushroom fruiting body is inhibited at high CO2, but the mechanism is poorly known. Fungal CO2 sensing may serve to position the spore-bearing tissue above the soil boundary layer to ensure effective spore dispersal. The animals that are most sensitive to anthropogenic CO2 enrichment are insects. Many insects have a well-developed ability to sense CO2 variation as a means of locating food. Unlike plants, insects have CO2 receptors that can detect variation in CO2 as low as 0.5 ppm. However, the sensitivity of these receptors is reduced in atmospheres with double or triple current levels of CO2, indicating some insect species may be threatened by rising atmospheric CO2.
Zooplankton egg banks are the accumulation of diapausing embryos of planktonic animals buried in the sediments of many aquatic ecosystems. These eggs, which are analogous life history stages to the seeds of many plants, can survive in a ready-to-hatch state for periods ranging from a few years to greater than a century. Their presence in ponds, lakes and near-shore marine environments has substantial implications for understanding trajectories of ecological and evolutionary change. When the sediments of lakes are structured in historical sequence, diapausing eggs extracted from different sediment ages can provide a means of studying past changes in community or population-genetic structure. A completely different aspect of egg banks derives from the fact that hatching of diapausing eggs can influence, through what can be thought of as temporal dispersal, population and community response to environmental change. Eggs hatching from diapause introduce to current environments species or genotypes laid at times in the distant past. In addition, egg banks create extended generation overlap that can play an important role in maintaining diversity in a fluctuating environment when different types (species or genotypes) are favored at different times. These distinct aspects of egg banks (i.e., their direct impact on ecological and evolutionary processes versus their usefulness in reconstructing historical changes), are potentially in conflict because for old eggs to hatch, the sediments must be at least partially mixed. This same mixing, however, degrades the accuracy of the historical record. Both aspects are possible, however, even within a single lake when sediment-mixing intensity is spatially heterogeneous.
The lack of mobility in plants is often interpreted as a sign of their passivity in the face of environmental variation. This view is perhaps most firmly entrenched with regard to water transport through the xylem in which water flows through the lumen of cells that are “dead” (i.e., lack any cytoplasm or nucleus) at maturity. However, recent work demonstrates that a number of active, physiological processes may be involved in maintaining the transport capacity of this essential pathway. Here we review work relating to both embolism repair and the effect of ion concentrations on xylem hydraulic properties as examples of such dynamic processes.
Even though water is required for the maintenance of biological integrity, numerous organisms are capable of surviving loss of virtually all their cellular water and existing in a state known as anhydrobiosis. Over the past three decades we and others have established that disaccharides such as trehalose and sucrose are almost certainly involved in stabilizing the dry cells. We discuss here some of the evidence behind the mechanism of this stabilization. Until the past few years this mechanism has been sufficiently appealing that a consensus has been developing that acquisition of these sugars in the cytoplasm may be both necessary and sufficient for anhydrobiosis. We show here that there are other routes to achieve the effects conferred by the sugars and that other adaptations are almost certainly required, at least in environmental conditions that are less than optimal. Under optimal storage conditions, the presence of the sugars alone may be sufficient to stabilize even mammalian cells in the dry state, findings that are already finding use in human clinical medicine.
STRESS-IS IT MORE THAN A DISEASE? A COMPARATIVE LOOK AT STRESS AND ADAPTATION
Stress involves real or perceived changes within an organism in the environment that activate an organism's attempts to cope by means of evolutionarily ancient neural and endocrine mechanisms. Responses to acute stressors involve catecholamines released in varying proportion at different sites in the sympathetic and central nervous systems. These responses may interact with and be complemented by intrinsic rythms and responses to chronic or intermittent stressors involving the hypothalamic-pituitary-adrenal axis. Varying patterns of responses to stressors are also affected by an animal's assessment of their prospects for successful coping. Subsequent central and systemic consequences of the stress response include apparent changes in affect, motivation, and cognition that can result in an altered relationship to environmental and social stimuli. This review will summarize recent developments in our understanding of the causes and consequences of stress. Special problems that need to be explored involve the manner in which ensembles of adaptive responses are assembled, how autonomic and neurohormonal reflexes of the stress response come under the influence of environmental stimuli, and how some specific aspects of the stress response may be integrated into the life history of a species.
Physical, chemical and perceived stressors can all evoke non-specific responses in fish, which are considered adaptive to enable the fish to cope with the disturbance and maintain its homeostatic state. If the stressor is overly severe or long-lasting to the point that the fish is not capable of regaining homeostasis, then the responses themselves may become maladaptive and threaten the fish's health and well-being. Physiological responses to stress are grouped as primary, which include endocrine changes such as in measurable levels of circulating catecholamines and corticosteroids, and secondary, which include changes in features related to metabolism, hydromineral balance, and cardiovascular, respiratory and immune functions. In some instances, the endocrine responses are directly responsible for these secondary responses resulting in changes in concentration of blood constituents, including metabolites and major ions, and, at the cellular level, the expression of heat-shock or stress proteins. Tertiary or whole-animal changes in performance, such as in growth, disease resistance and behavior, can result from the primary and secondary responses and possibly affect survivorship.
Fishes display a wide variation in their physiological responses to stress, which is clearly evident in the plasma corticosteroid changes, chiefly cortisol in actinopterygian fishes, that occur following a stressful event. The characteristic elevation in circulating cortisol during the first hour after an acute disturbance can vary by more than two orders of magnitude among species and genetic history appears to account for much of this interspecific variation. An appreciation of the factors that affect the magnitude, duration and recovery of cortisol and other physiological changes caused by stress in fishes is important for proper interpretation of experimental data and design of effective biological monitoring programs.
Research on the stress response in reptiles can provide a useful comparative perspective for understanding how the constituent elements of the response can be put into service of diverse behavioral adaptations. A summary of the neural and endocrine causes and consequences of specific behavioral patterns seen in the small diurnal lizard, Anolis carolinensis, has provided a model for the exploration of the dynamics of autonomic and neurohormonal contributions to adaptive behavior. In this species, changes in body color provide indices of the flux of circulating stress-relevant hormones, and are seen in situations from spontaneous exploration through agonistic behavior. Furthermore, captive adult males spontaneously and consistently manifest social dominance relationships that provide many of the elements of a stress-mediated adaptive behavioral patterns. These patterns include suppressed reproduction and long-term coping apparently based more on stress-mediated changes in motivation than acquired changes in behavior.
The hypothalamo-pituitary-adrenocortical (HPA) axis is recruited by the organism in response to real or perceived threats to homeostasis (“stress”). Regulation of this neuroendocrine system is accomplished by modulation of secretory tone in hypophysiotrophic neurons of the medial parvocellular paraventricular nucleus. Excitation of these neurons is mediated by several sources: direct (and perhaps indirect) inputs from brainstem neurons regulating autonomic tone/arousal; circumventricular organs monitoring blood and CSF constituents; and local-circuit neurons within the hypothalamus and basal forebrain. The latter are predominantly GABAergic; notably, these areas are targets for descending GABAergic input from limbic structures, and may promote PVN secretory activity via disinhibition. Neurosecretory paraventricular nucleus neurons are inhibited by glucocorticoid–dependent and –independent mechanisms. Glucocorticoid negative feedback appears to act both locally and in extrahypothalamic loci, and is likely integrated in a region- and stressor-specific manner. Inhibitory input to the medial parvocellular paraventricular nucleus emanate predominantly from the bed nucleus of the stria terminalis and hypothalamus, and are likely regulated by neuroendocrine homeostats. Descending limbic inhibitory information appears to act through excitation of these inhibitory inputs. Overall, integration of stressful information is a multi-faceted process integrating prior experience and real or anticipated homeostatic disruption into appropriate activation and deactivation of the hypothalamo-pituitary-adrenocortical axis.
Corticotropin releasing factor (CRF) is a critical integrator of the hypothalamic-pituitary-adrenal (HPA) axis in response to stress. CRF and its related molecule urocortin (UCN) bind CRF receptor 1 (CRFR1) and CRFR2 with distinct affinities. Mice deficient for CRFR1 or CRFR2 were generated in order to determine the physiological role of these receptors. While CRFR1-mutant mice show a depleted stress response and display anxiolytic-like behavior, CRFR2-mutant mice are hypersensitive to stress and display anxiogenic-like behavior. Both CRFR1- and CRFR2-mutant mice show normal basal feeding and weight gain, but CRFR2-mutant mice exhibit decreased food intake following a stress of food deprivation. While CRFR2-mutant mice display increased levels of CRF mRNA in the central nucleus of the amygdala (cAmyg) but not in the paraventricular nucleus of the hypothalamus (PVN), the CRFR1-mutant mice express high levels of CRF in the PVN but normal levels in the cAmyg. CRFR2-mutant mice also display increased levels of Ucn mRNA and protein in the edinger westphal nucleus (EW) as well as an increased number of cells expressing Ucn. The levels of these CRF-receptor ligands reflect the state of the receptor-deficient mice. These results demonstrate a possible modulatory function of CRFR2 in response to CRFR1 stimulation of the HPA axis or anxiety.
Stress may be defined as a sequence of events, that begins with a stimulus (stressor), that is recognized by the brain (stress perception), and which results in the activation of physiologic fight/flight/fright systems within the body (stress response). Many evolutionary selection pressures are stressors, and one of the primary functions of the brain is to perceive stress, warn the body of danger, and enable an organism to respond. We hypothesized that under acute conditions, just as the stress response prepares the cardiovascular and musculoskeletal systems for fight or flight, it may also prepare the immune system for challenges (e.g., wounding) which may be imposed by a stressor (e.g., an aggressor). Initial studies showed that acute (2h) stress induced a significant trafficking of immune cells to the skin. Since the skin is an organism's major protective barrier, we hypothesized that this leukocyte redistribution may serve to enhance skin immunity during acute stress. We tested this hypothesis using the delayed type hypersensitivity (DTH) reaction, which mediates resistance to various infectious agents, as a model for skin immune function. Acute stress administered immediately before antigen exposure significantly enhanced skin DTH. Adrenalectomy (ADX) eliminated the stress-induced enhancement of DTH while administration of physiological doses of corticosterone and/or epinephrine to ADX animals enhanced skin DTH in the absence of stress. These studies showed that changes in leukocyte distribution and circulating stress hormones are systemic mediators of the immunoenhancing effects of acute stress. We recently identified gamma interferon as a local cytokine mediator of a stress-induced immunoenhancement. Our results suggest that during acute stress the brain sends preparatory warning signals to the immune system just as it does to other fight/flight systems of the body.
Basal activity of the hypothalamo-pituitary-interrenal (HPI) axis changes over development in larval amphibians, but development of the responsiveness of this axis to an external stressor has not been studied. We compared developmental changes in whole-body corticosterone content of two anuran amphibian species, Rana pipiens (family Ranidae) and Xenopus laevis (family Pipidae). We also examined developmental changes in the responsiveness of the HPI axis by subjecting tadpoles of different developmental stages to a laboratory shaking/confinement stress and to ACTH injection. We measured whole-body corticosterone content as an indicator of the activity of the HPI axis. Whole-body corticosterone content of R. pipiens remained low during premetamorphosis and prometamorphosis but increased dramatically at metamorphic climax and remained elevated in juvenile frogs. By contrast, whole-body corticosterone content of X. laevis was highest during premetamorphosis, declined at the onset of prometamorphosis, increased at metamorphic climax and remained at climax levels in juvenile frogs. Premetamorphic and prometamorphic tadpoles of both species showed strong corticosterone responses to both shaking stress and ACTH injection. The magnitude and pattern of response differed among developmental stages, with premetamorphic tadpoles of both species showing greater responsiveness to stress and ACTH. Our results show that interrenal responsiveness is developed in premetamorphic tadpoles, suggesting that at these stages tadpoles are capable of mounting an increase in stress hormone production in response to changes in the external environment. Our results also highlight the importance of comparative studies in understanding the development of the stress axis.
Pacific salmon (genus Oncorhynchus) exhibit an interesting and uncommon life-history pattern that combines semelparity, anadromy, and navigation (homing). During smoltification, young salmon imprint on the chemical composition of their natal stream water (the home-stream olfactory bouquet or “HSOB”); they then migrate to the ocean where they spend a few years feeding prior to migrating back to their natal freshwater stream to spawn. Upstream migration is guided by the amazing ability to discriminate between the chemical compositions of different stream waters and thus identify and travel to their home-stream. Pacific salmon demonstrate marked somatic and neural degeneration changes during home-stream migration and at the spawning grounds. The appearance of these pathologies is correlated with a marked elevation in plasma cortisol levels. While the mechanisms of salmonid homing are not completely understood, it is known that adult salmon continuously utilize two of their primary sensory systems, olfaction and vision, during homing. Olfaction is the primary sensory system involved in freshwater homing and “HSOB” recognition, and will be emphasized here. Previously, we proposed that the increase in plasma cortisol during Pacific salmon home-stream migration is adaptive because it enhances the salmon's ability to recall the imprinted memory of the “HSOB” (Carruth, 1998; Carruth et al., 2000b). Elevated plasma concentrations of cortisol could prime the hippocampus or other olfactory regions of the brain to recall this memory and, therefore, aid in directing the fish to their natal stream. Thus, specific responses of salmon to stressors could enhance reproductive success.
Stress inhibits feeding behavior in all vertebrates. Data from mammals suggest an important role for hypothalamic neuropeptides, in particular the melanocortins and corticotropin-releasing hormone (CRH)-like peptides, in mediating stress-induced inhibition of feeding. The effects of CRH on food intake are evolutionarily ancient, as this peptide inhibits feeding in fishes, birds, and mammals. The effects of melanocortins on food intake have not been as extensively studied, but available evidence suggests that the anorexic role of neuronal melanocortins has been conserved. Although there is evidence that CRH and the melanocortins influence hypothalamic circuitry controlling food intake, these peptides may have a more primitive role in modulating visuomotor pathways involved in the recognition and acquisition of food. Stress rapidly reduces visually guided prey-catching behavior in toads, an effect that can be mimicked by administration of CRH, while corticosterone and isoproterenol are without effect. Melanocortins also reduce prey-oriented turning movements and, in addition, facilitate the acquisition of habituation to a moving prey item. The effects of these neuropeptides are rapid, occurring within 30 min after administration. Thus, changes in neuroendocrine status during stress may dramatically influence the efficacy with which visual stimuli release feeding behavior. By modulating visuomotor processing these neuropeptides may help animals make appropriate behavioral decisions during stress.
Behavioral interaction during social situations is a continuum of action, response, and reaction. The temporal nature of social interaction creates a series of stressful situations, such as aggression, displacement from resources, and the variable psychological challenge of adapting to dynamic social hierarchies. The ebb and flow of neurochemical and endocrine secretions during social stress provide a unique tool for understanding individualized responses to stress. Each social station is an adaptive response to a stressful social condition, resulting in unique neuroendocrine and behavioral responses. By examining the temporal changes of limbic monoamines and plasma glucocorticoids, aspects of mechanisms for adaptation emerge. The similarity of temporal patterns induced by social stress among fish, reptiles and primates are remarkable. Even different specific coping mechanisms point out the similarity of vertebrate stress responses. The lizard Anolis carolinensis exhibits a unique sign stimulus generated during social stress by the sympathetic nervous system that serves as a temporal landmark to distinguish neuroendocrine patterns. During social interaction dominant males have a shorter latency to eyespot darkening than opponents, inhibiting aggressive display. Eyespot coloration can be delayed using a serotonin reuptake inhibitor, causing dominant social status in many animals to be lost. Reversal of social status via serotonergic activation appears to mimic chronic serotonergic activity. The pattern of eyespot darkening, faster in dominant males, is coincident with that for serotonergic activity. The fundamental temporal relationship between dominant and subordinate limbic monoaminergic activity over a continuous course of social interaction appears to be a two-phase response, temporally specific to brain region, and always faster in dominant individuals.
In addition to seasonal changes in morphology, physiology and behavior that occur in predictable annual cycles, there are facultative responses to unpredictable events known as labile (i.e., short-lived) perturbation factors (LPFs). These rapid behavioral and physiological changes have been termed the “emergency” life history stage (ELHS) and serve to enhance life-time fitness. Glucocorticosteroids interacting with other hormones in the hypothalamo-pituitary-adrenal (HPA) cascade, initiate and orchestrate the ELHS within minutes to hours. Components of the ELHS include: redirection of behavior from a normal life history stage to increased foraging, irruptive-type migration during the day, enhanced restfulness at night, elevated gluconeogenesis and recovery once the perturbation passes. These physiological and behavioral changes allow an individual to avoid potential deleterious effects of stress that may result from chronically elevated levels of circulating glucocorticosteroids over days and weeks. In other words, acute rises in glucocorticosteroids following perturbations of the environment may actually avoid chronic stress and serve primarily as “anti-stress” hormones. Several field studies in diverse habitats indicate that free-living populations have elevated circulating levels of corticosteroids when in an ELHS. However, expression of an ELHS may not always be advantageous and there is accumulating evidence from birds that the adrenocortical responses to LPFs are modulated both on seasonal and individual levels. These data suggest that glucocorticosteroid secretions in response to LPFs not only trigger physiological and behavioral responses but also allow flexibility so that the response is integrated in relation to time of year (normal LHS) as well as individual differences owing to body condition, disease and social status.
LESSER-KNOWN PROTOSOME TAXA: EVOLUTION, DEVELOPMENT AND ECOLOGY
Most biologists are familiar only with a few of the approximately 40 extant animal phyla. The purpose of this symposium was to renew interest in the lesser-known invertebrate taxa, encourage their use in research and teaching and to promote the relevance of high-level systematic studies. This paper reviews the two major views of metazoan evolutionary relationships with particular attention to the lesser-known taxa and to some of the new and/or conflicting terminology used in current animal phylogenetic study. The current use of lesser-known taxa in research is briefly described, and the discussion that followed the symposium is summarized. The paper concludes with a brief history of the symposium and a tribute to Robert P. Higgins, who organized three “Symposia on the Lesser-Known Invertebrates” over the past 25 yr.
The article summarizes current knowledge mainly about the (functional) morphology and ultrastructure, but also about the biology, development, and evolution of the Kinorhyncha. The Kinorhyncha are microscopic, bilaterally symmetrical, exclusively free-living, benthic, marine animals and ecologically part of the meiofauna. They occur throughout the world from the intertidal to the deep sea, generally in sediments but sometimes associated with plants or other animals. From adult stages 141 species are known, but 38 species have been described from juvenile stages. The trunk is arranged into 11 segments as evidenced by cuticular plates, sensory spots, setae or spines, nervous system, musculature, and subcuticular glands. The ultrastructure of several organ systems and the postembryonic development are known for very few species. Almost no data are available about the embryology and only a single gene has been sequenced for a single species. The phylogenetic relationships within Kinorhyncha are unresolved. Priapulida, Loricifera, and Kinorhyncha are grouped together as Scalidophora, but arguments are found for every possible sistergroup relationship within this taxon. The recently published Ecdysozoa hypothesis suggests a closer relationship of the Scalidophora, Nematoda, Nematomorpha, Tardigrada, Onychophora, and Arthropoda.
Biodiversity research combines two dimensions, the horizontal one that contains species diversity, patterns among this diversity and its interconnections and the vertical one that deals with the history of biodiversity, i.e., its phylogeny. With these tight interconnections, the importance of so-called “lesser known groups” such as Nematomorpha and Gastrotricha can be shown. Two examples are the life cycle of Nematomorpha and the phylogenetic position of Gastrotricha. The life cycle of Nematomorpha is only partially known and almost no conclusions can be made about the impact of Nematomorpha on their hosts. For the phylogenetic position of Gastrotricha, alternative hypotheses are available, mainly due to different results of morphological and molecular (18S rDNA) analyses. It is demonstrated how these different hypotheses influence character interpretation and reconstruction among Protostomia (Gastroneuralia).
Loriciferans, cycliophorans and micrognathozoans are amongst the latest groups of animals to be discovered. Other than all being microscopic, they have very different body plans and are not closely related. Loriciferans were originally assigned to the Aschelminthes. However, both new molecular and ultrastructural researches have shown that Aschelminthes consist of two unrelated groups, Cycloneuralia and Gnathifera. Cycloneuralia may be included in the Ecdysozoa, including all molting invertebrates, and Gnathifera are more closely related to Platyhelminthes. The phylum Loricifera shares many apomorphic characters (e.g., scalids on the introvert) with both Priapulida and Kinorhyncha, and can be included in the taxon Scalidophora, a subgroup of Cycloneuralia. Cycliophora was originally allied to the Entoprocta and Ectoprocta (Bryozoa) based on ultrastructual research. Subsequent molecular data show they may be related to Rotifera and Acanthocephala, within the taxon Gnathifera. The phylogenetic position of Cycliophora is therefore not settled, and more ultrastructural and molecular data are needed. Micrognathozoa is the most recent major group of animals to be described. They show strong affinities with both Rotifera and Gnathostomulida (within the taxon Gnathifera), especially in the fine structure of the pharyngeal apparatus, where the jaw elements have cuticular rods with osmiophilic cores. Furthermore the micrognathozoans have two rows of multiciliated cells that form a locomotory organ, similar to that seen in some gastrotrichs and interstitial annelids. This character is never seen in Rotifera or in the monociliated Gnathostomulida. Rotifera and Acanthocephala always have a syncytial epidermis (Syndermata). Micrognathozoa lack this characteristic feature. Therefore, they are postulated to be placed basally in the Gnathifera, either as a sister-group to Gnathostomulida or as a sister-group to Rotifera Acanthocephala.
The Tardigrada are bilaterally symmetrical micrometazoans with four pairs of lobopod legs terminating in claws or sucking disks. They occupy a diversity of niches in marine, freshwater, and terrestrial environments throughout the world. Some have a cosmopolitan distribution, while others are endemic. About 900 species have been described thus far, but many more species are expected as additional habitats are investigated. Most are less than 1 mm in body length and are opaque or translucent, exhibiting colors such as brown, green, orange, yellow, red, or pink in the cuticle and/or gut. Marine species are more variable in body shape and overall appearance and generally exhibit low population density with high species diversity. Reproductive modes include sexual reproduction and parthenogenesis, but much remains to be known about development. Tardigrades have a hemocoel-type of fluid-filled body cavity, a complete digestive tract, and a lobed dorsal brain with a ventral nerve cord with fused ganglia. Recent molecular analyses and additional morphological studies of the nervous system have confirmed the phylogenetic position of tardigrades as a sister group of the arthropods. The ability of tardigrades to undergo cryptobiosis has long intrigued scientists. Although tardigrades are active only when surrounded by a film of water, they can enter latent states in response to desiccation (anhydrobiosis), temperature (cryobiosis), low oxygen (anoxybiosis), and salinity changes (osmobiosis). Cryptobiotic states aid in dispersal.
Rotifers comprise a modestly sized phylum (≈1,850 species) of tiny (ca. 50–2,000 μm), bilaterally symmetrical, eutelic metazoans, traditionally grouped within the pseudocoelomates or Aschelminthes. These saccate to cylindrically shaped protostomes possess three prominent regions (corona, trunk, foot). They are distinguished by a ciliated, anterior corona (used in locomotion and food gathering) and a pharynx equipped with a complex set of jaws. Unfortunately, these generalizations grossly oversimplify a rich and fascinating diversity. Chief among the charms of the study of rotifers are their ecological importance, ease of culture (including chemostat technology), and the fact that much remains unknown about this exquisite phylum.
The study of parasite evolution relies on the identification of free-living sister taxa of parasitic lineages. Most lineages of parasitic helminths are characterized by an amazing diversity of species that complicates the resolution of phylogenetic relationships. Acanthocephalans offer a potential model system to test various long-standing hypotheses and generalizations regarding the evolution of parasitism in metazoans. The entirely parasitic Acanthocephala have a diversity of species that is manageable with regards to constructing global phylogenetic hypotheses, exhibit variation in hosts and habitats, and are hypothesized to have close phylogenetic affinities to the predominately free-living Rotifera. In this paper, I review and test previous hypotheses of acanthocephalan phylogenetic relationships with analyses of the available 18S rRNA sequence database. Maximum-parsimony and maximum-likelihood inferred trees differ significantly with regard to relationships among acanthocephalans and rotifers. Maximum-parsimony analysis results in a paraphyletic Rotifera, placing a long-branched bdelloid rotifer as the sister taxon of Acanthocephala. Maximum-likelihood analysis results in a monophyletic Rotifera. The difference between the two optimality criteria is attributed to long-branch attraction. The two analyses are congruent in terms of relationships within Acanthocephala. The three sampled classes are monophyletic, and the Archiacanthocephala is the sister taxon of a Palaeacanthocephala Eoacanthocephala clade. The phylogenetic hypothesis is used to assess the evolution of host and habitat preferences. Acanthocephalan lineages have exhibited multiple radiations into terrestrial habitats and bird and mammal definitive hosts from ancestral aquatic habitats and fish definitive hosts, while exhibiting phylogenetic conservatism in the type of arthropod intermediate host utilized.
In traditional classification schemes, the Annelida consists of the Polychaeta and the Clitellata (the latter including the Oligochaeta and Hirudinida). However, recent analyses suggest that annelids are much more diverse than traditionally believed, and that polychaetes are paraphyletic. Specifically, some lesser-known taxa (previously regarded as separate phyla) appear to fall within the annelid radiation. Abundant molecular, developmental, and morphological data show that the Siboglinidae, which includes the formerly recognized Pogonophora and Vestimentifera, are derived annelids; recent data from the Elongation Factor-1α (EF-1α) gene also suggest that echiurids are of annelid ancestry. Further, the phylogenetic origins of two other lesser-known groups of marine worms, the Myzostomida and Sipuncula, have recently been called into question. Whereas some authors advocate annelid affinities, others argue that these taxa do not fall within the annelid radiation. With advances in our understanding of annelid phylogeny, our perceptions of body plan evolution within the Metazoa are changing. The evolution of segmentation probably is more plastic than traditionally believed. However, as our understanding of organismal evolution is being revised, we are also forced to reconsider the specific characters being examined. Should segmentation be considered a developmental process or an ontological endpoint?
Ectoprocts, phoronids and brachiopods are often dealt with under the heading Tentaculata or Lophophorata, sometimes with entoprocts discussed in the same chapter, for example in Ruppert and Barnes (1994). The Lophophorata is purported to be held together by the presence of a “lophophore,” a mesosomal tentacle crown with an upstream-collecting ciliary band. However, the mesosomal tentacle crown of pterobranchs has upstream-collecting ciliary bands with monociliate cells, similar to those of phoronids and brachiopods, although its ontogeny is not well documented. On the contrary, the ectoproct tentacle crown carries a ciliary sieving system with multiciliate cells and the body does not show archimery, neither during ontogeny nor during budding, so the tentacles cannot be characterized as mesosomal. The entoprocts have tentacles without coelomic canals and with a downstream-collecting ciliary system like that of trochophore larvae and adult rotifers and serpulid and sabellid annelids. Planktotrophic phoronid and brachiopod larvae develop tentacles at an early stage, but their ciliary system resembles those of echinoderm and enteropneust larvae. Ectoproct larvae are generally non-feeding, but the planktotrophic cyphonautes larvae of certain gymnolaemates have a ciliary band resembling that of the adult tentacles. The entoprocts have typical trochophore larvae and many feed with downstream-collecting ciliary bands. Phoronids and brachiopods are thus morphologically on the deuterostome line, probably as the sister group of the “Neorenalia” or Deuterostomia sensu stricto. The entoprocts are clearly spiralians, although their more precise position has not been determined. The position of the ectoprocts is uncertain, but nothing in their morphology indicates deuterostome affinities. “Lophophorata” is thus a polyphyletic assemblage and the word should disappear from the zoological vocabulary, just as “Vermes” disappeared many years ago.
This paper reviews progress in developmental biology and phylogeny of the Nemertea, a common but poorly studied spiralian taxon of considerable ecological and evolutionary significance. Analyses of reproductive biology (including calcium dynamics during fertilization and oocyte maturation), larval morphology and development and developmental genetics have significantly extended our knowledge of spiralian developmental biology. Developmental genetics studies have in addition provided characters useful for reconstructing metazoan phylogeny. Reinvestigation of the cell lineage of Cerebratulus lacteus using fluorescent tracers revealed that endomesoderm forms from the 4d cell as in other spiralians and that ectomesoderm is derived from the 3a and 3b cells as in annelids, echiurans and molluscs. Studies examining blastomere specification show that cell fates are established precociously in direct developers and later in indirect developers. Morphological characters used to estimate the phylogenetic position of nemerteans are critically re-evaluated, and cladistic analyses of morphology reveal that conflicting hypotheses of nemertean relationships result because of different provisional homology statements. Analyses that include disputed homology statements (1, gliointerstitial cell system 2, coelomic circulatory system) suggest that nemerteans form the sister taxon to the coelomate spiralian taxa rather than the sister taxon to Platyhelminthes. Analyses of small subunit rRNA (18S rDNA) sequences alone or in combination with morphological characters support the inclusion of the nemerteans in a spiralian coelomate clade nested within a more inclusive lophotrochozoan clade. Ongoing evaluation of nemertean relationships with mitochondrial gene rearrangements and other molecular characters is discussed.