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The Bartholomew Award has now completed a decade of recognizing outstanding young investigators in comparative physiology and biochemistry or in related fields of functional and integrative biology. It honors Professor George A. Bartholomew (Bart to his many students and other friends), whose research contributions continue to be important in shaping these fields. Bart's influence reflects a steadfast adherence to a set of basic precepts: the inherent unity of biology; the need for an evolutionary perspective in functional studies; the value of modern natural history in guiding research investigations; the focus on the organism and its function in nature, even in highly reductionist studies; the importance of biological variability within and between species; and the crucial interactions of physiology and behavior in allowing animals to deal with environmental challenges. Were he to have done nothing else in his career, he would remain an important figure in the fields with which the Society of Integrative and Comparative Biology's (SICB) Division of Comparative Physiology and Biochemistry is concerned. However, his influence is also felt through his inspirational performance as an undergraduate teacher, his skill and wisdom as a graduate mentor, his many services to the University of California, his insightful contributions to scientific committees and policy boards at the national level, and his presidency of the American Society of Zoologists (now SICB). This symposium offers the opportunity for honoring Bart for all his accomplishments and fine personal qualities, while illustrating the contributions of the impressive set of younger investigators who are recipients of the George A. Bartholomew Award.
The colors of deep-sea species are generally assumed to be cryptic, but it is not known how cryptic they are and under what conditions. This study measured the color of approximately 70 deep-sea species, both pelagic and benthic, and compared the results with two sets of predictions: 1) optimal crypsis under ambient light, 2) optimal crypsis when viewed by bioluminescent “searchlights.” The reflectances of the pelagic species at the blue-green wavelengths important for deep-sea vision were far lower than the predicted reflectances for crypsis under ambient light and closer to the zero reflectance prediction for crypsis under searchlights. This suggests that bioluminescence is more important than ambient light for the visual detection of pelagic species at mesopelagic depths. The reflectances of the benthic species were highly variable and a relatively poor match to the substrates on which they were found. However, estimates of the contrast sensitivity of deep-sea visual systems suggest that even approximate matches may be sufficient for crypsis in visually complex benthic habitats. Body coloration was generally uniform, but many crabs had striking patterns that may serve to disrupt the outlines of their bodies.
The goal of my research program is to employ biochemical and molecular techniques to gain ecological insight into the role of temperature in setting species' distribution patterns in the marine environment. Our central focus is the study of the environmental regulation of gene expression, where we are particularly interested in a set of inducible molecular chaperones, the heat-shock proteins (Hsps), and how the expression of these genes varies with the thermal history of organisms in natural populations. The primary study organisms are intertidal invertebrates and marine fish that experience dramatic changes in body temperature on varying temporal and spatial scales. In this review, I present studies that address the variable expression of Hsps, how these genes are differentially regulated in ectothermic animals in response to ecologically relevant temperature conditions, and how such plasticity in gene expression contributes to physiological plasticity in the environment.
We introduce the concept of many-to-one mapping of form to function and suggest that this emergent property of complex systems promotes the evolution of physiological diversity. Our work has focused on a 4-bar linkage found in labrid fish jaws that transmits muscular force and motion from the lower jaw to skeletal elements in the upper jaws. Many different 4-bar shapes produce the same amount of output rotation in the upper jaw per degree of lower jaw rotation, a mechanical property termed Maxillary KT. We illustrate three consequences of many-to-one mapping of 4-bar shape to Maxillary KT. First, many-to-one mapping can partially decouple morphological and mechanical diversity within clades. We found with simulations of 4-bars evolving on phylogenies of 500 taxa that morphological and mechanical diversity were only loosely correlated (R2 = 0.25). Second, redundant mapping permits the simultaneous optimization of more than one mechanical property of the 4-bar. Labrid fishes have capitalized on this flexibility, as illustrated by several species that have Maxillary KT = 0.8 but have different values of a second property, Nasal KT. Finally, many-to-one mapping may increase the influence of historical factors in determining the evolution of morphology. Using a genetic model of 4-bar evolution we exerted convergent selection on three different starting 4-bar shapes and found that mechanical convergence only created morphological convergence in simulations where the starting forms were similar. Many-to-one mapping is widespread in physiological systems and operates at levels ranging from the redundant mapping of genotypes to phenotypes, up to the morphological basis of whole-organism performance. This phenomenon may be involved in the uneven distribution of functional diversity seen among animal lineages.
Social interactions in small groups of juvenile rainbow trout (Oncorhynchus mykiss) lead to the formation of dominance hierarchies. Dominant fish hold better positions in the environment, gain a larger share of the available food and exhibit aggression towards fish lower in the hierarchy. By contrast, subordinate fish exhibit behavioural inhibition, including reduced activity and feeding. The behavioural characteristics associated with social status are likely the result of changes in brain monoamines resulting from social interactions. Whereas substantial physiological benefits, including higher growth rates and condition factor, are experienced by dominant trout, low social status appears to be a chronic stress, as indicated by sustained elevation of circulating cortisol concentrations in subordinate fish. High cortisol levels, in turn, may be responsible for many of the deleterious physiological consequences of low social status, including lower growth rates and condition factor, immunosuppression and increased mortality. Circulating cortisol levels may also be a factor in determining the outcome of social interactions in pairs of rainbow trout, and hence in determining social status. Rainbow trout treated with cortisol were significantly more likely to become subordinate in paired encounters with smaller untreated conspecifics.
Fruit flies alter flight direction by generating rapid, stereotyped turns, called saccades. The successful implementation of these quick turns requires a well-tuned orchestration of neural circuits, musculo-skeletal mechanics, and aerodynamic forces. The changes in wing motion required to accomplish a saccade are quite subtle, as dictated by the inertial dynamics of the fly's body. A fly first generates torque to begin accelerating in the intended direction, but then must quickly create counter-torque to decelerate. Several lines of evidence suggest that the initial turn is initiated by visual expansion, whereas the subsequent counter-turn is triggered by the gyroscopic halteres. This integrated analysis indicates how the functional organization of neural circuits controlling behavior is rigidly constrained by the physical interaction between an animal and the external world.
Vertebrate intestinal tracts possess an array of structural and functional adaptations to the wide diversity of food and feeding habits. In addition to well-described differences in form and function between herbivores and carnivores, the intestine exhibits adaptive plasticity to variation in digestive demand. The capacity to which intestinal performance responds to changes in digestive demands is a product of evolutionary and cellular mechanisms. In this report, I have taken an integrative approach to exploring the mechanisms responsible for the regulation of intestinal performance with feeding and fasting among amphibians and reptiles. Intestinal performance is presented as the total small intestinal capacity to absorb nutrients, quantified as a product of small intestinal mass and mass-specific rates of nutrient uptake. For sit-and-wait foraging snakes and estivating anurans, both of which naturally experience long episodes of fasting, the dramatic downregulation of intestinal morphology and function with fasting reduces energy expenditure during extended fasts. In contrast, frequently-feeding species modestly regulate intestinal performance with fasting and feeding, trading higher basal rates of metabolism during fasting for the frequent expense of upregulating the gut with feeding. Surveying the magnitude by which intestinal uptake capacity is regulated among 26 families of amphibians and reptiles has revealed potentially five lineages that have independently evolved the capacity to widely regulate intestinal performance. The extent to which intestinal performance is downregulated with fasting among amphibians and reptiles, ranging from 0 to 90%, is largely a function of the degree by which mass-specific rates of nutrient transport are depressed, given that loss of intestinal mass with fasting is a common characteristic of vertebrates. In exploring the underlying mechanisms regulating intestinal nutrient uptake, use of the Burmese python has revealed a temporal match between microvillus surface area and intestinal nutrient transport. With feeding, pythons experience a five-fold lengthening of intestinal microvilli, with subsequent reduction after completing digestion. Identifying for the python the cellular processes responsible for the dramatic remodeling of the microvilli would assist in elucidating the mechanisms by which intestinal performance is regulated, as well as identify whether similar steps are employed by other species to regulate their intestines. In finishing, I propose three studies of digestive response: (1) investigate the responses of the ectotherm intestine to hibernation; (2) evaluate whether functional capacities of tissues are matched to digestive demands; and, (3) apply microarray technology to explore the functional genomics of intestinal adaptation.
Billions of songbirds migrate between continents each year, but we have yet to obtain enough information on in-flight physiology and energetics to fully understand the migratory behavior of any one species. New World Catharus thrushes are common nocturnal migrants amenable to biotelemetry, allowing us to measure physiological parameters during migratory flight in the wild. Here, we review work by the authors on Catharus thrush in-flight physiology during spring migration in continental North America and present new data on individual variation in energy use during migratory flight. Previous work demonstrated that (1) a number of simple behavioral rules are sufficient to explain the initiation of individual migratory flights made by Catharus thrushes, (2) the thrushes used a magnetic compass to orient during the night rather than celestial cues and that they calibrated this magnetic compass each day using cues associated with the setting sun, (3) in total, Catharus thrushes used approximately twice as much energy during stopovers than they used during migratory flight, and (4) thrushes may use more energy when thermoregulating on cold days than on days when they make short migratory flights. Recently, we built upon this work and used newly-developed transmitters to measure heart rate, wingbeat frequency and respiration rate of free-flying Swainson's Thrushes (C. ustulatus). We found a large amount of between-individual variation in average heart rate after ascent (range 12.06–14.81 Hz, mean ± SD, 13.48 ± 0.75, n = 10), average wingbeat frequency after ascent (10.25–11.75 Hz, 10.82 ± 0.49, n = 10), and the difference between the two variables (1.5–3.84 Hz, 2.53 ± 0.76, n = 8). Both heart rate and wingbeat frequency were significantly higher during ascent than later in the flight. We propose biotelemetry as a means to understand energetic trade-offs and decisions during natural migratory flight in songbirds. To further our knowledge of intercontinental songbird migration and the connectivity between wintering and breeding sites, we outline plans for a satellite-based global tracking system for <1 g transmitters.
Top pelagic predators such as tunas, sharks, marine turtles and mammals have historically been difficult to study due to their large body size and vast range over the oceanic habitat. In recent years the development of small microprocessor-based data storage tags that are surgically implanted or satellite-linked provide marine researchers a novel avenue for examining the movements, physiology and behaviors of pelagic animals in the wild. When biological and physical data obtained from the tags are combined with satellite derived sea surface temperature and ocean color data, the relationships between the movements, behaviors and physical ocean environment can be examined. Tag-bearing marine animals can function as autonomous ocean profilers providing oceanographic data wherever their long migrations take them. The biologging science is providing ecological physiologists with new insights into the seasonal movements, habitat utilization, breeding behaviors and population structures in of marine vertebrates. In addition, the data are revealing migration corridors, hot spots and physical oceanographic patterns that are key to understanding how organisms such as bluefin tunas use the open ocean environment. In the 21st century as ecosystem degradation and global warming continue to threaten the existence of species on Earth, the field of physiological ecology will play a more pivotal role in conservation biology.
Concern continues to grow over the negative impact of endocrine disrupting chemicals on environmental and public health. The number of identified endocrine disrupting chemicals is increasing, but biological endpoints, experimental design, and approaches for examining and assessing the impact of these chemicals are still debated. Although some workers consider endocrine disruption an “emerging science,” I argue here that it is equally, a “merging science” developing in the tradition of integrative biology. Understanding the impact of endocrine disruptors on humans and wildlife is an examination of “context dependent development” and one that Scott Gilbert predicted would require a “new synthesis” or a “revolution” in the biological sciences. Here, I use atrazine as an example to demonstrate the importance of an integrative approach in understanding endocrine disruptors.
Atrazine is a potent endocrine disruptor that chemically castrates and feminizes amphibians and other wildlife. These effects are the result of the induction of aromatase, the enzyme that converts androgens to estrogens, and this mechanism has been confirmed in all vertebrate classes examined (fish, amphibians, reptiles, birds, and mammals, including humans). To truly assess the impact of atrazine on amphibians in the wild, diverse fields of study including endocrinology, developmental biology, molecular biology, cellular biology, ecology, and evolutionary biology need to be invoked. To understand fully the long-term impacts on the environment, meteorology, geology, hydrology, chemistry, statistics, mathematics and other disciplines well outside of the biological sciences are required.
The last common ancestor to all extant animals possessed features shared between the most basal metazoan lineage—Porifera—and the rest of the animal kingdom. To identify ancient and conserved developmental processes, we have been investigating embryogenesis and metamorphosis in the demosponge Reniera. Many of the cardinal features of eumetazoan development are displayed during Reniera embryogenesis. Specifically, after fertilization there is a period of cell division with little to no cell growth that results in two obvious cell populations distinguished by size as micromeres and macromeres, and by fate: the small cells differentiate into ciliated cells. This is followed by a period of differential cell activities that produces an embryo consisting of two then three layers, where at least 11 populations of differentiated cells are allocated into the different layers and patterned within these layers. This organization yields a swimming larva with the capacity to sense and respond to the surrounding environment, despite a lack of neurons and a coordinating system. During Reniera embryogenesis, the clearest example of cell patterning is the formation of a ring of pigment cells at the future posterior pole of the larva. Pigment cell pattern formation has two phases, both of which may require the movement of a large number of cells apparently in response to a morphogen gradient. First, pigmented cells, which initially cover the surface of the embryo, migrate to the future posterior end and form a dark spot. Second, the cells move outwards from the spot and rearrange into a ring. Numerous and diverse transcription factor genes are expressed during Reniera embryogenesis, most of which belong to metazoan-specific families and include members of POU, LIMHD, Pax, Bar, Prox2, NK-2, T-box, MEF-2, Fox, Sox, Ets, and nuclear hormone receptor families. In combination, these observations suggest that the last common ancestor to all extant metazoan lineages already possessed the basic regulatory genetic architecture to direct the specification, patterning and differentiation of multiple cell types. Some of these differentiated cells may have been arranged into localised functional units—i.e., simple tissues.
Haeckel's studies of development in calcareous sponges (1872) led him to develop the “Gastraea Theory,” which proposes that the ancestral mode of germ layer formation, or gastrulation, was by invagination to produce a functional gut. His observations that gastrulation in the Calcarea occurs by invagination of a ciliated larva upon settlement and metamorphosis were supported by remarkable photomicrographs of the stage by Hammer in 1908. Although no later work found the same stage, these concepts are repeated in texts today. We have re-examined embryogenesis and metamorphosis in Sycon sp. cf. S. raphanus in order to understand when gastrulation occurs. Almost all larvae settle on their ciliated anterior pole and metamorphose into a bilayered juvenile whose interior cells rapidly differentiate into choanocytes and other cells of the young sponge. After a four-year search we have found the transitory stage shown by Hammer in which the anterior cells invaginate into the posterior half of the larva. The hole closes and it is not until some days later that the sponge forms an osculum at its apical pole. To understand whether invagination comprises gastrulation and if the hole can be considered to be a blastopore we have carried out a review of the literature dealing with this brief moment in calcaronean sponge development. Despite the intrigue of this type of metamorphosis, we conclude that gastrulation occurs earlier, during formation of the two cellular regions of the larva, and that metamorphosis involves the reorganization of these already differentiated regions. Considering the pivotal position occupied by the Calcarea as the possible sister-group to all other Metazoa, these results call for a reassessment of germ layer formation and of the relationships of the primary germ layers among basal metazoan phyla.
On Caribbean coral reefs, some sponge species produce chemical defenses, while others do not and are non-fatally grazed by predatory fishes. It has been hypothesized that the latter may compensate for fish grazing by growing faster or rapidly healing wounds. Rates of wound-healing were measured for chemically defended and undefended tubular and vase-shaped sponges on patch reefs in the Florida Keys and Bahamas in 2002. Healing rates were significantly faster during the first few days of the experiment, with rates leveling off after the third day. Chemically undefended sponges healed at significantly faster rates (Callyspongia plicifera, 8% area regenerated per day; Callyspongia vaginalis, 6%; Niphates digitalis, 6%; Xestospongia muta, 6.5%) than chemically defended sponges (Cribrochalina vasculum, 2%; Ircinia campana, 2%; Verongula gigantea, 0%). Orientation of wounds relative to the tidal current had no influence on healing rates. Specimens of Niphates digitalis growing in tubular form had faster healing rates than individuals with vasiform shapes. Our results suggest that Caribbean reef sponges followed two different evolutionary trajectories: chemically defended species deter fish predation and have slow healing rates, while chemically undefended species allocate resources to rapid wound-healing in response to grazing.
Sponges are important components of marine benthic communities of Antarctica. Numbers of species are high, within the lower range for tropical latitudes, similar to those in the Arctic, and comparable or higher than those of temperate marine environments. Many have circumpolar distributions and in some habitats hexactinellids dominate benthic biomass. Antarctic sponge assemblages contribute considerable structural heterogeneity for colonizing epibionts. They also represent a significant source of nutrients to prospective predators, including a suite of spongivorous sea stars whose selective foraging behaviors have important ramifications upon community structure. The highly seasonal plankton blooms that typify the Antarctic continental shelf are paradoxical when considering the planktivorous diets of sponges. Throughout much of the year Antarctic sponges must either exploit alternate sources of nutrition such as dissolved organic carbon or be physiologically adapted to withstand resource constraints. In contrast to predictions that global patterns of predation should select for an inverse correlation between latitude and chemical defenses in marine sponges, such defenses are not uncommon in Antarctic sponges. Some species sequester their defensive metabolites in the outermost layers where they are optimally effective against sea star predation. Secondary metabolites have also been shown to short-circuit molting in sponge-feeding amphipods and prevent fouling by diatoms. Coloration in Antarctic sponges may be the result of relict pigments originally selected for aposematism or UV screens yet conserved because of their defensive properties. This hypothesis is supported by the bioactive properties of pigments examined to date in a suite of common Antarctic sponges.
The marine sponge Lamellodysidea chlorea contains large populations of the host-specific, filamentous cyanobacterium Oscillatoria spongeliae. Other marine sponges, including Xestospongia exigua, contain the generalist, unicellular cyanobacterium Synechococcus spongiarum. The impact of cyanobacterial photosynthesis on host sponges was manipulated by shading these sponge-cyanobacteria associations. If cyanobacteria benefit their hosts, shading should reduce this benefit. Chlorophyll a concentrations were measured as an index of cyanobacterial abundance. After two weeks, shaded L. chlorea lost more mass than controls, while shaded and control X. exigua did not lose a significant amount of mass. Chlorophyll a concentrations in shaded X. exigua were lower than in controls, but were not significantly different between shaded and control L. chlorea. In addition, L. chlorea shaded in situ lost over 40% of their initial area, but did not differ in chlorophyll a concentrations from controls. These results suggest that Oscillatoria symbionts benefit their host sponges in a mutualistic association. Synechococcus symbionts may be commensals that exploit the resources provided by their sponge hosts without significantly affecting sponge mass. When shaded, Synechococcus symbionts may be consumed by their hosts or may be able to disperse from this unfavorable environment. These data support the hypothesis that more specialized symbionts provide a greater benefit to their hosts, but hypotheses concerning the dispersal abilities of these symbionts remain to be explored. Sponge-cyanobacteria symbioses provide model systems for investigating the costs and benefits of symbiosis and the roles of dispersal, environmental conditions, and phylogenetic history in determining the specificity of endosymbionts for their hosts.
Marine sponges are an ecologically important and highly diverse component of marine benthic communities, found in all the world's oceans, at all depths. Although their commercial potential and evolutionary importance is increasingly recognized, many pivotal aspects of their basic biology remain enigmatic. Knowledge of historical biogeographic affinities and biodiversity patterns is rudimentary, and there are still few data about genetic variation among sponge populations and spatial patterns of this variation. Biodiversity analyses of tropical Australasian sponges revealed spatial trends not universally reflected in the distributions of other marine phyla within the Indo-West Pacific region. At smaller spatial scales sponges frequently form heterogeneous, spatially patchy assemblages, with some empirical evidence suggesting that environmental variables such as light and/or turbidity strongly contribute to local distributions. There are no apparent latitudinal diversity gradients at larger spatial scales but stochastic processes, such as changing current patterns, the presence or absence of major carbonate platforms and historical biogeography, may determine modern day distributions. Studies on Caribbean oceanic reefs have revealed similar patterns, only weakly correlated with environmental factors. However, several questions remain where molecular approaches promise great potential, e.g., concerning connectivity and biogeographic relationships. Studies to date have helped to reveal that sponge populations are genetically highly structured and that historical processes might play an important role in determining such structure. Increasingly sophisticated molecular tools are now being applied, with results contributing significantly to a better understanding of poriferan microevolutionary processes and molecular ecology.