Unitary Organisms Research Articles

Degradation of a Sauce-Glazed Ware from the Song Dynasty Salvaged Out of Water at the Dalian Island Wharf: Part II—The Effect of Surface-Attached Marine Organism Remains

Dalian Island, located in the northwest of Pingtan County, Fujian Province, China, has been an important junction on the Maritime Silk Road since the Tang dynasty. This study focuses on sauce-glazed ceramic ware from the Song dynasty salvaged from the waters near Dalian Island Wharf. The composition, phase attributes, and microstructures of the marine organism remains attached to the ceramic ware were analyzed using an optical microscope, scanning electron microscope, and micro-Raman spectrometer to investigate the influence of marine organisms on the degradation of the ceramic ware. Long-term abrasion by sea wave-borne debris led to the increased surface roughness and wettability of the ceramic ware, facilitating the attachment of marine organisms. Differences in surface roughness between the inner and outer walls led to varying levels of biomass. Coralline algae secreted inducers to attract the larvae of macrofoulers. The attachment of different types of marine organisms had varying effects on the degradation of the ceramic ware. Firmly attached unitary organisms could alleviate the scouring of sea wave-borne debris and hinder the intrusion of foreign pollutants, thereby playing a ‘bio-protective’ role. In contrast, the group skeletons of modular organisms could reinforce the mechanically damaged surface but failed to block the intrusion of iron rust and other pollutants, resulting in chemical alterations of the glaze. Therefore, the specific species of the attached marine organisms should be considered in subsequent conservation efforts.

Aligning spatial ecological theory with the study of clonal organisms: the case of fungal coexistence.

Established ecological theory has focused on unitary organisms, and thus its concepts have matured into a form that often hinders rather than facilitates the ecological study of modular organisms. Here, we use the example of filamentous fungi to develop concepts that enable integration of non-unitary (modular) organisms into the established community ecology theory, with particular focus on its spatial aspects. In doing so, we provide a link between fungal community ecology and modern coexistence theory (MCT). We first show how community processes and predictions made by MCT can be used to define meaningful scales in fungal ecology. This leads to the novel concept of the unit of community interactions (UCI), a promising conceptual tool for applying MCT to communities of modular organisms with indeterminate clonal growth and hierarchical individuality. We outline plausible coexistence mechanisms structuring fungal communities, and show at what spatial scales and in what habitats they are most likely to act. We end by describing challenges and opportunities for empirical and theoretical research in fungal competitive coexistence.

Effect of a generalist mesopredator on modular and unitary sessile prey associated with a foundation species.

Unitary and modular sessile organisms both dominate in marine benthic communities, commonly preyed upon by the same generalist predators. The differences between unitary and modular defensive strategies may underlie the ways generalist predators control community structure, but this has never been empirically examined. We hypothesize that the individual size of an omnivorous mesopredatory shrimp affects the relative vulnerability of unitary and modular prey and hence translates into community structure. In a short-term laboratory microcosm experiment, we assessed the effect of the shrimp individual size on an epibiotic assemblage of red algae blades initially dominated by three species of modular bryozoans and a unitary serpulid tubeworm. We found that the individual size of a shrimp determines its effect on the prey community composition. Large shrimp stronger than small shrimp increased the proportion of unitary tubeworms among the epibionts surviving predation. While large shrimp reduced the proportions of all the three dominant bryozoan species, small shrimp, in contrast, mostly increased the proportion of a bryozoan species with the smallest modules and largest colonies. This bryozoan, like the tubeworms, demonstrated a higher survival rate with larger individual (colony) size. Yet, against large shrimp this bryozoan was outperformed by the largest tubeworms almost immune to predation. Partial predation by small shrimp modestly improved survival of the largest bryozoan colonies. Thus, relative vulnerability of unitary and modular prey is determined by the predator individual size. Our findings clarify the complex way the size structures of generalist consumers and their prey shape communities by affecting the species-specific relative performance of modular and unitary organisms. The demography of a foundation species and the competitive hierarchy can have additional effects by altering the balance of predation and competition.

Metabolic scaling as an emergent outcome of variation in metabolic rate.

The allometric scaling of metabolic rate and what drives it are major questions in biology with a long history. Since the metabolic rate at any level of biological organization is an emergent property of its lower-level constituents, it is an outcome of the intrinsic heterogeneity among these units and the interactions among them. However, the influence of lower-level heterogeneity on system-level metabolic rate is difficult to investigate, given the tightly integrated body plan of unitary organisms. In this context, social insects such as honeybees can serve as important model systems because unlike unitary organisms, these superorganisms can be taken apart and reassembled in different configurations to study metabolic rate and its various drivers at different levels of organization. This commentary discusses the background of such an approach and how combining it with artificial selection to generate heterogeneity in metabolic rate with an analytical framework to parse out the different mechanisms that contribute to the effects of heterogeneity can contribute to the various models of metabolic scaling. Finally, the absence of the typical allometric scaling relationship among different species of honeybees is discussed as an important prospect for deciphering the role of top-down ecological factors on metabolic scaling. This article is part of the theme issue 'The evolutionary significance of variation in metabolic rates'.

Ultrastructural and immunocytochemical evidence of a colonial nervous system in hydroids.

As the sister group to all Bilateria, representatives of the phylum Cnidaria (sea anemones, corals, jellyfishes, and hydroids) possess a recognizable and well-developed nervous system and have attracted considerable attention over the years from neurobiologists and evo-devo researchers. Despite a long history of nervous system investigation in Cnidaria, most studies have been performed on unitary organisms. However, the majority of cnidarians are colonial (modular) organisms with unique and specific features of development and function. Nevertheless, data on the nervous system in colonial cnidarians are scarce. Within hydrozoans (Hydrozoa and Cnidaria), a structurally "simple" nervous system has been described for Hydra and zooids of several colonial species. A more complex organization of the nervous system, closely related to the animals' motile mode of life, has been shown for the medusa stage and a few siphonophores. Direct evidence of a colonial nervous system interconnecting zooids of a hydrozoan colony has been obtained only for two species, while it has been stated that in other studied species, the coenosarc lacks nerves. In the present study, the presence of a nervous system in the coenosarc of three species of colonial hydroids - the athecate Clava multicornis, and thecate Dynamena pumila and Obelia longissima - was studied based on immunocytochemical and ultrastructural investigations. Confocal scanning laser microscopy revealed a loose system composed of delicate, mostly bipolar, neurons visualized using a combination of anti-tyrosinated and anti-acetylated a-tubulin antibodies, as well as anti-RF-amide antibodies. Only ganglion nerve cells were observed. The neurites were found in the growing stolon tips close to the tip apex. Ultrastructural data confirmed the presence of neurons in the coenosarc epidermis of all the studied species. In the coenosarc, the neurons and their processes were found to settle on the mesoglea, and the muscle processes were found to overlay the nerve cells. Some of the neurites were found to run within the mesoglea. Based on the findings, the possible role of the colonial nervous system in sessile hydroids is discussed.

The novel Orshina Rhythm in a colonial urochordate signifies the display of recurrent aging/rejuvenation sequels

When it comes to aging, some colonial invertebrates present disparate patterns from the customary aging phenomenon in unitary organisms, where a single senescence phenomenon along ontogeny culminates in their inevitable deaths. Here we studied aging processes in 81 colonies of the marine urochordate Botryllus schlosseri each followed from birth to death (over 720 days). The colonies were divided between three life history strategies, each distinct from the others based on the presence/absence of colonial fission: NF (no fission), FA (fission develops after the colony reaches maximal size), and FB (fission develops before the colony reaches maximal size). The study revealed recurring patterns in sexual reproductive statuses (hermaphroditism and male-only settings), colonial vigor, and size. These recurring patterns, collectively referred to as an Orshina, with one or more 'astogenic segments' on the genotype level. The combination of these segments forms the Orshina rhythm. Each Orshina segment lasts about three months (equivalent to 13 blastogenic cycles), and concludes with either the colonial death or rejuvenation, and is manipulated by absence/existing of fission events in NF/FA/FB strategies. These findings indicate that reproduction, life span, death, rejuvenation and fission events are important scheduled biological components in the constructed Orshina rhythm, a novel aging phenomenon.

Coming of age: Annual onset of coral reproduction is determined by age rather than size

Constraints on organisms possessing a unitary body plan appear almost absent from colonial organisms. Like unitary organisms, however, coral colonies seemingly delay reproduction until reaching a critical size. Elucidating ontogenetic processes, such as puberty and aging are complicated by corals' modular design, where partial mortality and fragmentation lead to distortions in colony size-age relationships. We explored these enigmatic relations and their influence on reproduction by fragmenting sexually mature colonies of five coral species into sizes below the known size at first reproduction, nurturing them for prolonged periods, and examining their reproductive capacity and trade-offs between growth rates and reproductive investment. Most fragments were reproductive regardless of their size, and growth rates hardly affected reproduction. Our findings suggest that once the ontogenetic milestone of puberty is reached, corals retain reproductive capacity irrespective of colony size, highlighting the key role that aging may have in colonial animals, which are commonly considered non-aging.

Ontogeny of collective behaviour.

During their lifetime, superorganisms, like unitary organisms, undergo transformations that change the machinery of their collective behaviour. Here, we suggest that these transformations are largely understudied and propose that more systematic research into the ontogeny of collective behaviours is needed if we hope to better understand the link between proximate behavioural mechanisms and the development of collective adaptive functions. In particular, certain social insects engage in self-assemblage, forming dynamic and physically connected architectures with striking similarities to developing multicellular organisms, making them good model systems for ontogenetic studies of collective behaviour. However, exhaustive time series and three-dimensional data are required to thoroughly characterize the different life stages of the collective structures and the transitions between these stages. The well-established fields of embryology and developmental biology offer practical tools and theoretical frameworks that could speed up the acquisition of new knowledge about the formation, development, maturity and dissolution of social insect self-assemblages and, by extension, other superorganismal behaviours. We hope that this review will encourage an expansion of the ontogenetic perspective in the field of collective behaviour and, in particular, in self-assemblage research, which has far-reaching applications in robotics, computer science and regenerative medicine. This article is part of a discussion meeting issue 'Collective behaviour through time'.

Modularity and connectivity of nest structure scale with colony size.

Large body sizes have evolved structures to facilitate resource transport. Like unitary organisms, social insect colonies must transport information and resources. Colonies with more individuals may experience transport challenges similar to large-bodied organisms. In ant colonies, transport occurs in the nest, which may consist of structures that facilitate movement. We examine three attributes of nests that might have evolved to mitigate transport challenges related to colony size: (1) subdivision-nests of species with large colonies are more subdivided to reduce crowd viscosity; (2) branching-nest tunnels increase branching in species with large colonies to reduce travel distances; and (3) shortcuts-nests of species with large colonies have cross-linking tunnels to connect distant parts of the nest and create alternative routes. We test these hypotheses by comparing nest structures of species with different colony sizes in phylogenetically controlled meta-analyses. Our findings support the hypothesis that nest subdivision and branching evolved to mitigate transport challenges related to colony size. Nests of species with large colonies contain more chambers and branching tunnels. The similarity in how ant nests and bodies of unitary organisms have evolved in response to increasing size suggests common solutions across taxa and levels of biological organization.

The use of plant ontologies in comparative and evolutionary studies should be flexible

The use of plant ontologies in comparative and evolutionary studies should be flexible

Marine invertebrate epibionts on photophilic seaweeds: importance of algal architecture

The macrofauna of marine invertebrates of two photophilic algal communities on the Maresme coast (Barcelona, NE Spain) were studied. We evaluated how the type of algal substrate (soft or hard thallus algae) affects the distribution patterns of organisms living in them. Quantitative samples were collected in the months of October 2013 and February 2014 at 15-m depth by scraping standard surfaces of 400 cm2. A total of 164 specific or supraspecific taxa were obtained and grouped into two categories: unitary and modular organisms. Of the 118 taxa of unitary organisms, a total of 4587 specimens were counted: 2029 were arthropods (44.2%), 1284 were polychaete annelids (27.9%), and 1080 were mollusks (23.54%). The unitary organisms were counted and weighed and were used for most of the statistical and biodiversity analyses. For the modular organisms, 46 different taxa belonging to Porifera, Hydrozoa, Bryozoa, and Tunicata were identified. Modular organisms were studied only at a qualitative level. In soft thallus algae, a greater abundance of epibiont invertebrates was found, but with lower biomass than in calcareous algae, while the latter showed a greater species richness and Shannon-Wiener index. In general, we can conclude that the nature (soft or hard thallus) and architecture (branched or crusted) of the macroalgae can limit the size and abundance of the epibiont invertebrates and can condition the populations of organisms that settle in them.

Partitioning colony size variation into growth and partial mortality.

Body size is a trait that broadly influences the demography and ecology of organisms. In unitary organisms, body size tends to increase with age. In modular organisms, body size can either increase or decrease with age, with size changes being the net difference between modules added through growth and modules lost through partial mortality. Rates of colony extension are independent of body size, but net growth is allometric, suggesting a significant role of size-dependent mortality. In this study, we develop a generalizable model of partitioned growth and partial mortality and apply it to data from 11 species of reef-building coral. We show that corals generally grow at constant radial increments that are size independent, and that partial mortality acts more strongly on small colonies. We also show a clear life-history trade-off between growth and partial mortality that is governed by growth form. This decomposition of net growth can provide mechanistic insights into the relative demographic effects of the intrinsic factors (e.g. acquisition of food and life-history strategy), which tend to affect growth, and extrinsic factors (e.g. physical damage, and predation), which tend to affect mortality.

Testing Finch's hypothesis: The role of organismal modularity on the escape from actuarial senescence

Abstract Until recently, senescence was assumed to be a universal phenomenon. Evolutionary theories of senescence predict that no organism may escape the physiological decline that results in an increase in mortality risk and/or decline in fertility with age. However, evidence both in animals and plants has emerged in the last decade defying such predictions. Researchers are currently seeking mechanistic explanations for the observed variation in ageing trajectories. We argue that the historical view on the inevitability of senescence is due, in part, to the development of its classical theories, which targeted primarily unitary organisms. In unitary species, the integration of resources and functions is high, and adult size is determined. In contrast, the architecture of modular organisms is indeterminate and built upon repeated modules. The isolation of mortality risk in species like hydra (Hydra spp.) or creosote brush Larrea tridentata may explain their null or even negative senescence. Caleb Finch hypothesized three decades ago that species with the ability to compartmentalize risk may escape senescence. Here, we first review the evidence on organisms that slow down or even avoid senescence in the context of their architecture, along a continuum of unitarity‐modularity. Then, we use open‐access databases to comparatively analyse various moments of senescence and link longevity to the degree of anatomical modularity. Our analysis compares the pace of senescence across 138 plants and 151 animals, and the shape of senescence across a subset of these. Our comparative analysis reveals that plant species that are more modular do indeed tend to escape from senescence more often than those that are unitary. The role of modularity in animal senescence is less clear. In light of novel support for Finch's hypothesis across a large diversity of plant species, and with less conclusive findings in animals, we identify new research directions. We highlight the opportunities related to age‐dependent mortality factors. Other areas for further research include the role of modularity in relation to endocrine actions, and the costs of modular anatomies.

Fussy groups thwart the collective burden of choice: A theoretical study of house-hunting ants

Information is crucial to effective decision making, but too much information can be as detrimental as too little. Pooling information allows group-living organisms to benefit from the ‘wisdom of the crowds’, but could also increase the risk of information overload if not complemented by increased information processing capacity. In this study I use an agent-based model and empirical tests to explore the influence of group-size on information accumulation, and the impact of this on collective decision-making. Larger groups were more effective at sampling the environment in simulations and empirical trials. Simulations suggest this this could render them more susceptible to information overload in candidate-rich environments, in which larger groups suffered delays to decision making because of poorly focussed information sharing. However, the cost of excessive information could be ameliorated if individuals are ‘fussy’ and filter information by withholding information on poor candidates. This may explain observations from empirical trials, in which higher rates of information accumulation in larger groups did not have a clear impact on decision making. These results suggest groups face a potential collective burden of choice from excessive novel information in complex environments. However, collective information-filtering mechanisms analogous to those in the brains of unitary organisms could allow groups to exploit the wisdom of the crowds without suffering from information overload.

Cope's Rule in a modular organism: Directional evolution without an overarching macroevolutionary trend.

Cope's Rule describes increasing body size in evolutionary lineages through geological time. This pattern has been documented in unitary organisms but does it also apply to module size in colonial organisms? We address this question using 1169 cheilostome bryozoans ranging through the entire 150 million years of their evolutionary history. The temporal pattern evident in cheilostomes as a whole shows no overall change in zooid (module) size. However, individual subclades show size increases: within a genus, younger species often have larger zooids than older species. Analyses of (paleo)latitudinal shifts show that this pattern cannot be explained by latitudinal effects (Bergmann's Rule) coupled with younger species occupying higher latitudes than older species (an “out of the tropics” hypothesis). While it is plausible that size increase was linked to the advantages of large zooids in feeding, competition for trophic resources and living space, other proposed mechanisms for Cope's Rule in unitary organisms are either inapplicable to cheilostome zooid size or cannot be evaluated. Patterns and mechanisms in colonial organisms cannot and should not be extrapolated from the better‐studied unitary organisms. And even if macroevolution simply comprises repeated rounds of microevolution, evolutionary processes occurring within lineages are not always detectable from macroevolutionary patterns.

Increased investment in the defence of high-value offspring by a superorganism

Parental investment theory predicts that parents should adjust their investment in offspring defence according to offspring value (i.e. the probability they will contribute to the next generation). Although previous research has shown this offspring value prediction is generally supported in unitary organisms, the ‘superorganisms’ formed by advanced colonial organisms have rarely been tested, and never by direct manipulation of offspring value. As an important complement to correlational studies, such a test would help better illuminate the applicability of the parental investment theory to that higher level of biological organization, as well as provide insight into the depth of the superorganism analogy. Here I use colonies of the fire ant, Solenopsis invicta, in a manipulative experiment to test whether superorganisms behave as predicted by the parental investment theory and invest more in defence (deliver larger venom doses) when protecting higher-value offspring. In addition, to test a proposed mechanism for observed increases, I conducted an experiment to investigate whether S. invicta alarm pheromone modulates venom dose. I found that colonies delivered larger venom doses when defending nests containing higher-value (sexual) offspring than when defending worker-destined brood, but I found no venom dose increase as a result of additional alarm pheromone. The conformity of S. invicta colonies to the offspring value prediction of the parental investment theory supports the theory's applicability to their higher (superorganismal) level of animal organization. It furthermore underscores that the superorganism concept is deeper than simple anatomical/organizational analogy, but extends also to colony-level behaviour.

Towards an understanding of the evolutionary role of fire in animals

Wildfires underpin the dynamics and diversity of many ecosystems worldwide, and plants show a plethora of adaptive traits for persisting recurrent fires. Many fire-prone ecosystems also harbor a rich fauna; however, knowledge about adaptive traits to fire in animals remains poorly explored. We review existing literature and suggest that fire is an important evolutionary driver for animal diversity because (1) many animals are present in fire-prone landscapes and may have structural and phenotypic characters that contribute to adaptation to these open landscapes; and (2) in some cases, animals from fire-prone ecosystems may show specific fire adaptations. While there is limited evidence on morphological fire adaptations in animals, there is evidence suggesting that different behaviors might provide a rich source of putative fire adaptations; this is because, in contrast to plants, most animals are mobile, unitary organisms, have reduced survival when directly burnt by fire and can move away from the fire. We call for research on fire adaptations (morphological, behavioral, and physiological) in animals, and emphasize that in the animal kingdom many fire adaptations are likely to be behavioral. While it may be difficult to discern these adaptations from other animal behaviors, making this distinction is fundamental if we want to understand the role of fire in shaping biodiversity. Developing this understanding is critical to how we view and manage our ecosystems in the face of current global and fire regime changes.

Temperature effects on mass-scaling exponents in colonial animals: a manipulative test.

Body size and temperature are fundamental drivers of ecological processes because they determine metabolic rates at the individual level. Whether these drivers act independently on individual-level metabolic rates remains uncertain. Most studies of intraspecific scaling of unitary organisms must rely on preexisting differences in size to examine its relationship with metabolic rate, thereby potentially confounding size-correlated traits (e.g., age, nutrition) with size, which can affect metabolic rate. Here, we use a size manipulation approach to test whether metabolic mass scaling and temperature dependence interact in four species (two phyla) of colonial marine invertebrates. Size manipulation in colonial organisms allows tests of how ecological processes (e.g., predation) affect individual physiology and consequently population- and community-level energy flux. Body mass and temperature interacted in two species, with one species exhibiting decreased and the other increased mass-scaling exponents with increasing temperature. The allometric scaling of metabolic rate that we observe in three species contrasts with the isometric scaling of ingestion rates observed in some colonial marine invertebrates. Thus, we suggest that the often observed competitive superiority of colonial over unitary organisms may arise because the difference between energy intake and expenditure increases more strongly with size in colonial organisms.

Life‐history strategy and behavioral type: risk‐tolerance reflects growth rate and energy allocation in ant colonies

Despite the recent interest in animal personality and behavioral syndromes, there is a paucity of explanations for why distinct behavioral traits should evolve to correlate. We investigate whether such correlations across apparently distinct behavioral traits may be explained by variation in life history strategy among individual ant colonies. Life history theory predicts that the way in which individuals allocate energy towards somatic maintenance or reproduction drives several distinct traits in physiology, morphology, and energy use; it also predicts that an individual's willingness to engage in risky behaviors should depend on reproductive strategy.We use Temnothorax ants, which have been shown to exhibit ‘personalities’ and a syndrome that may reflect risk tolerance at the colony level. We measure colonies' relative investment in growth rate (new workers produced) compared to reproductive effort (males and queens produced). Comparing sterile worker production to reproductive alate production provides a direct measure of how colonies are investing their energy, analogous to investment in growth versus reproduction in a unitary organism. Consistently with this idea, we found that behavioral type of ant colonies was associated with their life history strategy: risk‐tolerant colonies grew faster and invested more in reproduction, whereas risk‐averse colonies had lower growth rate but invested relatively more in workers. This provides evidence that behavioral syndromes can be a consequence of life‐history strategy variation, linking the two fields and supporting the use of an integrative approach.

Extreme polygyny in the previously unstudied subtropical ant Temnothorax tuscaloosae with implications for the biogeographic study of the evolution of polygyny

Evolutionary ecologists often seek to explain life history variation at geographical scales. Progress in this regard has been slower in social insects than in unitary organisms, due in part to limited information about species distributions and the complexity of studying colony-level traits. Temnothorax ants have proven useful for investigating associations between ecology and life history traits in ants, because they have small colonies ( 400 species that range from temperate to tropical biomes. Here, we generate the first global map of Temnothorax diversity and demonstrate that previous ecological hypotheses for colony life history variation in the genus are based on data and studies confined to a small part of the overall genus-level distribution. For example, studies of northern-latitude species have suggested that overwintering success is a prominent selective force favoring polygyny but little is known about polygyny in Temnothorax species from other regions. We report the highest observed queen numbers known in the genus in the subtropical species T. tuscaloosae and confirm that all queens in these polygynous colonies are mated and actively laying eggs. Behavioral laboratory experiments further indicate that this species has a fluid nest structure and lacks intraspecific aggression at the whole-forest scale. These results extend the biogeographical extent of life history studies for this genus and point to evolutionary discoveries awaiting comparative research of the global Temnothorax fauna.