Further exploration into the adaptive design of the arthropod "microbrain": I. Sensory and memory-processing systems

Arthropods have small but sophisticated brains that have enabled them to adapt their behavior to a diverse range of environments. In this review, we first discuss some of general characteristics of the arthropod "microbrain" in comparison with the mammalian "megalobrain". Then we discuss about recent progress in the study of sensory and memory-processing systems of the arthropod "microbrain". Results of recent studies have shown that (1) insects have excellent capability for elemental and context-dependent forms of olfactory learning, (2) mushroom bodies, higher olfactory and associative centers of arthropods, have much more elaborated internal structures than previously thought, (3) many genes involved in the formation of basic brain structures are common among arthropods and vertebrates, suggesting that common ancestors of arthropods and vertebrates already had organized head ganglia, and (4) the basic organization of sensori-motor pathways of the insect brain has features common to that of the mammalian brain. These findings provide a starting point for the study of brain mechanisms of elaborated behaviors of arthropods, many of which remain unexplored.     

Notes from Underground: Towards Ultimate Hypotheses of Cyclic, Discontinuous Gas-Exchange in Tracheate Arthropods

SYNOPSIS. The Discontinuous Gas-exchange Cycle or DGC is generallythought to have evolved primarily as a means of reducing respiratorywater loss rates in tracheate arthropods. However, several linesof evidence suggest that this supposition is oversimplified.I suggest that the DGC originated as an adaptation to the hypoxicand hypercapnic environments characteristic of underground burrows,rather than primarily as an adaptation to reduce respiratorywater loss rates. This suggestion is based on a considerationof trans-spiracular oxygen and carbon dioxide partial pressuregradients in such environments, and the concomitant importanceof decoupling oxygen and carbon dioxide exchange. The occurrenceand/ or absence of the DGC in sundry arthropod taxa is discussed,and diverse phylogenetic and other arguments are advanced forthe inferred distribution thereof.     

ARTHROPODS THAT PREY ON VERTEBRATES

1. Many arthropods are predators of vertebrates: four orders of the class arachnida, six orders of insecta, five orders of crustacea and one order of chilopoda include species that have been reported to eat vertebrates. At the population level, some arthropods are responsible for significant mortality among some vertebrates.
2. Arthropods are well equipped for this type of predation; many are larger than vertebrates (approximately 20% of the vertebrate fauna of eastern North America is less than 10 cm in length), they may hunt in social groups and many have toxins or other adaptations that increase predatory efficiency.
3. Several arthropod predators and vertebrates may be involved in cross predation, the species eating each other. The switch in the role of predator and prey occurs during 'ontogenetic reversal' as the vertebrate grows from small and vulnerable to large and predaceous. Cross predation decreases the future risk for one's self or offspring.
4. The opportunity for arthropod predation on vertebrates exists in many communities, but a review of some food webs catalogued by Cohen (1978) indicates that this particular link may be easily overlooked. Some arthropods should be investigated as potential predators of vertebrates.
5. The information available from the analysis of feeding interactions in a community should be an important link between field and theoretical ecology; however, most food webs are probably underestimates of the complexity that is commonplace.     

Harmfulness of parasitic insects and acarines to mammals and birds

The paper summarizes the results of investigations on the harmfulness of the blood-sucking arthropods and ectoparasites to terrestrial vertebrates. Pathogenicity of parasitic arthropods strongly depends on the type of parasitism. Harmfulness to the hosts is analyzed separately in blood-sucking dipterans, ixodid ticks, gadflies, and both temporary (fleas and bugs) and permanent (biting lice, lice, acariform mites) ectoparasites. The pathogenicity of parasitic arthropods for the host organism is conditioned by the direct loss of blood and tissues, toxic effect of the arthropod’s saliva, and allergic reactions. Indirect injury from parasites is associated with deterioration of the host’s nutrition and loss of weight and viability. Pathogenicity for the host not resulting in its death is typical of parasitic arthropods, except for heavy attacks by blood-sucking Diptera which may lead to death of domesticated and wild animals. Most data on the pathogenicity of arthropods for vertebrates refer to domesticated animals. Annual losses to the world livestock breeding attributed to insects and acarines amount to several billion dollars. Direct evidence of ectoparasite pathogenicity to wild animals and effect on the host’s vital functions, reproduction, and population numbers in particular, is limited and unconvincing.     

Contrasting tactics in motor control by vertebrates and arthropods

Vertebrates and arthropods share the common problem of controllinga rigid, articulated skeleton using neurally-controlled, striatedmuscle. Since this condition has arisen independently in thetwo groups, there is no reason to assume, a priori, that thecontrol mechanisms used by the two groups will be the same.Indeed, there appear to be fundamental differences in the tacticsused by the two groups. Insects and crustaceans use small numbersof heterogeneous motoneurons, while vertebrates (mammals especially)use many, more homogeneous, motor axons. In particular, arthropodsmake extensive use of peripheral neuromodulation to alter theproperties of both neuromuscular junctions and muscle fibers.There has been little consideration of the functional consequencesof these differences. I suggest that, faced with a size constrainton the number of motor units available, arthropods use peripheralmodulation of muscle properties to achieve the flexibility anddynamic range that vertebrates achieve through recruitment ofmotor units.     

Diverged and conserved aspects of heart formation in a spider

Heart development exhibits some striking similarities between vertebrates and arthropods, for example in both cases the heart develops as a linear tube from mesodermal cells. Furthermore, the underlying molecular pathways exhibit a significant number of similarities between vertebrates and the fruit fly Drosophila, suggesting a common origin of heart development in the last common ancestor of flies and vertebrates. However, there is hardly any molecular data from other animals. Here we show that many of the key genes are also active in heart development in the spider Cupiennius salei. Spiders belong to the chelicerates and are distantly related to insects with respect to the other arthropods. The tinman/Nkx2.5 ortholog is the first gene to be specifically expressed in the presumptive spider heart, like in flies and vertebrates. We also show that tinman is expressed in a similar way in the beetle Tribolium castaneum. Taken together this demonstrates that tinman has a conserved role in the specification of the arthropod heart. In addition, we analyzed the expression of other heart genes (decapentaplegic, Wnt5, H15, even-skipped, and Mef2 ) in Cupiennius. The expression of these genes suggests that the genetic pathway of heart development may be largely conserved among arthropods. However, a major difference is seen in the earlier expression of the even-skipped gene in the developing spider heart compared with Drosophila, implying that the role of even-skipped in heart formation might have changed during arthropod evolution. The most striking finding, however, is that in addition to the dorsal tissue of the fourth walking leg segment and the opisthosomal segments, we discovered tinman-expressing cells that arise from a position dorsal to the cephalic lobe and that contribute to the anterior dorsal vessel. In contrast to the posterior heart tissue, these cells do not express the other heart genes. The spider heart thus is composed of two distinct populations of cells.     

Delta-Notch signalling in segmentation

Modular body organization is found widely across multicellular organisms, and some of them form repetitive modular structures via the process of segmentation. It's vastly interesting to understand how these regularly repeated structures are robustly generated from the underlying noise in biomolecular interactions. Recent studies from arthropods reveal similarities in segmentation mechanisms with vertebrates, and raise the possibility that the three phylogenetic clades, annelids, arthropods and chordates, might share homology in this process from a bilaterian ancestor. Here, we discuss vertebrate segmentation with particular emphasis on the role of the Notch intercellular signalling pathway. We introduce vertebrate segmentation and Notch signalling, pointing out historical milestones, then describe existing models for the Notch pathway in the synchronization of noisy neighbouring oscillators, and a new role in the modulation of gene expression wave patterns. We ask what functions Notch signalling may have in arthropod segmentation and explore the relationship between Notch-mediated lateral inhibition and synchronization. Finally, we propose open questions and technical challenges to guide future investigations into Notch signalling in segmentation.     

Decoupling elongation and segmentation: Notch involvement in anostracan crustacean segmentation

Repeated body segments are a key feature of arthropods. The formation of body segments occurs via distinct developmental pathways within different arthropod clades. Although some species form their segments simultaneously without any accompanying measurable growth, most arthropods add segments sequentially from the posterior of the growing embryo or larva. The use of Notch signaling is increasingly emerging as a common feature of sequential segmentation throughout the Bilateria, as inferred from both the expression of proteins required for Notch signaling and the genetic or pharmacological disruption of Notch signaling. In this study, we demonstrate that blocking Notch signaling by blocking γ‐secretase activity causes a specific, repeatable effect on segmentation in two different anostracan crustaceans, Artemia franciscana and Thamnocephalus platyurus. We observe that segmentation posterior to the third or fourth trunk segment is arrested. Despite this marked effect on segment addition, other aspects of segmentation are unaffected. In the segments that develop, segment size and boundaries between segments appear normal, engrailed stripes are normal in size and alignment, and overall growth is unaffected. By demonstrating Notch involvement in crustacean segmentation, our findings expand the evidence that Notch plays a crucial role in sequential segmentation in arthropods. At the same time, our observations contribute to an emerging picture that loss‐of‐function Notch phenotypes differ significantly between arthropods suggesting variability in the role of Notch in the regulation of sequential segmentation. This variability in the function of Notch in arthropod segmentation confounds inferences of homology with vertebrates and lophotrochozoans.     

Trophic cascades in tropical rainforests: Effects of vertebrate predator exclusion on arthropods and plants in Papua New Guinea

Insect herbivores have the potential to consume large amounts of plant tissue in tropical forests, but insectivorous vertebrates effectively control their abundances, indirectly increasing plant fitness accordingly. Despite several studies already sought understanding of the top-down effects on arthropod community structure and herbivory, such studies of trophic cascades in old tropics are underrepresented, and little attention was paid to top-down forces in various habitats. Therefore, we examine how flying insectivorous vertebrates (birds and bats) impact arthropods and, consequently, affect herbivore damage of leaves in forest habitats in Papua New Guinea. In a 3-month long predator exclosure experiment conducted at four study sites across varying elevation and successional stage, we found that vertebrate predators reduced arthropod density by ∼52%. In addition, vertebrate predators decreased the mean body size of arthropods by 26% in leaf chewers and 47% in non-herbivorous arthropods but had only a small effect on mesopredators and sap suckers. Overall, the exclusion of vertebrate predators resulted in a ~ 41% increase in leaf damage. Our results, across different types of tropical forests in Papua New Guinea, demonstrate that flying vertebrate insectivores have a crucial impact on plant biomass, create a selective pressure on larger and non-predatory prey individuals and they prey partition with mesopredators.     

The ABC gene family in arthropods: Comparative genomics and role in insecticide transport and resistance

About a 100 years ago, the Drosophila white mutant marked the birth of Drosophila genetics. The white gene turned out to encode the first well studied ABC transporter in arthropods. The ABC gene family is now recognized as one of the largest transporter families in all kingdoms of life. The majority of ABC proteins function as primary-active transporters that bind and hydrolyze ATP while transporting a large diversity of substrates across lipid membranes. Although extremely well studied in vertebrates for their role in drug resistance, less is known about the role of this family in the transport of endogenous and exogenous substances in arthropods. The ABC families of five insect species, a crustacean and a chelicerate have been annotated in some detail. We conducted a thorough phylogenetic analysis of the seven arthropod and human ABC protein subfamilies, to infer orthologous relationships that might suggest conserved function. Most orthologous relationships were found in the ABCB half transporter, ABCD, ABCE and ABCF subfamilies, but specific expansions within species and lineages are frequently observed and discussed. We next surveyed the role of ABC transporters in the transport of xenobiotics/plant allelochemicals and their involvement in insecticide resistance. The involvement of ABC transporters in xenobiotic resistance in arthropods is historically not well documented, but an increasing number of studies using unbiased differential gene expression analysis now points to their importance. We give an overview of methods that can be used to link ABC transporters to resistance. ABC proteins have also recently been implicated in the mode of action and resistance to Bt toxins in Lepidoptera. Given the enormous interest in Bt toxicology in transgenic crops, such findings will provide an impetus to further reveal the role of ABC transporters in arthropods.     

The functional relationship between ectodermal and mesodermal segmentation in the crustacean, Parhyale hawaiensis

In arthropods, annelids and chordates, segmentation of the body axis encompasses both ectodermal and mesodermal derivatives. In vertebrates, trunk mesoderm segments autonomously and induces segmental arrangement of the ectoderm-derived nervous system. In contrast, in the arthropod Drosophila melanogaster, the ectoderm segments autonomously and mesoderm segmentation is at least partially dependent on the ectoderm. While segmentation has been proposed to be a feature of the common ancestor of vertebrates and arthropods, considering vertebrates and Drosophila alone, it is impossible to conclude whether the ancestral primary segmented tissue was the ectoderm or the mesoderm. Furthermore, much of Drosophila segmentation occurs before gastrulation and thus may not accurately represent the mechanisms of segmentation in all arthropods. To better understand the relationship between segmented germ layers in arthropods, we asked whether segmentation is an intrinsic property of the ectoderm and/or the mesoderm in the crustacean Parhyale hawaiensis by ablating either the ectoderm or the mesoderm and then assaying for segmentation in the remaining tissue layer. We found that the ectoderm segments autonomously. However, mesoderm segmentation requires at least a permissive signal from the ectoderm. Although mesodermal stem cells undergo normal rounds of division in the absence of ectoderm, they do not migrate properly in respect to migration direction and distance. In addition, their progeny neither divide nor express the mesoderm segmentation markers Ph-twist and Ph-Even-skipped. As segmentation is ectoderm-dependent in both Parhyale and holometabola insects, we hypothesize that segmentation is primarily a property of the ectoderm in pancrustacea.     

Impact of Entomopathogenic Nematodes on Non-target Hosts

Biological pest control has been thought to be ecologically safe for many years. More recently, it has been questioned whether entomopathogens and beneficial arthropods or nematodes truly have no impact on non-target species. Only a few studies deal with the action of entomopathogenic nematodes on non-target animals, although a broad spectrum of species has been tested in the laboratory. Entomopathogenic nematodes do not affect vertebrates under natural conditions. Mortality caused by the release of entomopathogenic nematodes among non-target arthropod populations can occur, but will only be temporary, will be spatially restricted and will affect only part of a population. In plots treated with entomopathogenic nematodes, the impact on the non-target fauna proved to be negligible. The possible impact of introduced exotic nematode species is discussed and regulatory measures for the release are proposed.     

Types of parasitism of acarines and insects on terrestrial vertebrates

According to the recent taxonomic revisions, over 40000 species of insects and acarines are parasites or micropredatory blood-suckers of mammals and birds. The largest fraction of them are micropredators and temporary or permanent ectoparasites, the minority being endoparasitic. Some arthropods (blood-sucking dipterans) use the host primarily as a food resource, whereas for others (many astigmatic mites) the host constitutes the entire environment. A number of life forms, or types of parasitism, have arisen in the insects and acarines in the course of their adaptive evolution to parasitism on terrestrial vertebrates. The term “type of parasitism” designates a set of convergently arising morpho-physiological and ecological adaptations (adaptive complexes), demonstrated by different arthropod taxa. A classification of the types of parasitism in arthropods is proposed based on their temporal, spatial, and trophic associations with vertebrates. The following seven types of parasitism are distinguished: micropredatory blood-suckers, nest ectoparasites (nidicoles), temporary ectoparasites with prolonged feeding, permanent ectoparasites, intracutaneous endoparasites, cavity endoparasites, and tissue endoparasites.     

Plasma membrane specializations in resting, stimulated and phagocytosing arthropod (Limulus polyphemus, Gromphadorhina portentosa and Blattella germanica) immunocytes: structural and functional analogies with those of vertebrate macrophages and neutrophils

Using indirect immunofluorescence and scanning electron microscope techniques, we have shown that the plasma membrane specializations, such as pseudopods, filopods, lamellipods, and zeiotic blebs occur in activated and/or phagocytosing arthropod (Limulus polyphemus, Gromphadorhina portentosa, and Blattella germanica) immunocytes (hemocytes), as they do in challenged vertebrate neutrophils and macrophages. All four specializations may also be caused by some of the chemicals in the preparative media, which suggests that arthropod immunocytes, like the vertebrate neutrophils and macrophages, have evolved as highly reactive cells that are sensitive to chemical and/or biological foreign agonists/antigens. These attributes are necessary for the effectiveness of a cellular defense mechanism. The plasma membrane specializations perform the same functions in arthropod immunocytes as reported for those of vertebrates. For example, pseudopods and lamellipods are needed for spreading and locomotion and filopodia for cell adhesion and crawling. Because they are formed as a result of similar reactions to foreign antigens, as in vertebrate cells, it is suggested that similar terminologies be consistently used for them in arthropods.     

Vertebrate golgi complexes have beads in a similar position to those found in arthropods

Insects and other arthropods have bead-like structures in Golgi complexes from all cell types. They are arranged in rings at the base of transition vesicles located near the smooth surface of the rough endoplasmic reticulum making the forming face of the Golgi complex and are only seen easily after staining in bismuth salts. Procedures used to demonstrate the beads in arthropod Golgi complexes do not selectively stain any structures where they would be expected to occur in several mouse and tadpole tissues. However, a faint pattern similar to the arthropod GC beads can be made out in the large GCs concerned in the formation of acrosomes during mouse spermatogenesis. Uranyl staining shows particles of about the same size and spacing as the beads of arthropod GCs. We conclude that vertebrate GCs may have beads that differ from arthropods in their staining properties.     

Ultrastructure and Development of the Laticifers of Ficus carica L

Laticifers of Ficus caricaL. are of the branched, non-articulatedtype. They occur in the cortex and pith of the plant axis andpenetrate leaves and inflorescences. Observations were madeon laticifers located in shoot apices. Growing regions of laticifers undergo a sequence of ultrastructuralchanges. These are: (a) a pronounced increase in the vacuolarspace which divides the cytoplasm into separated masses; (b)a development of numerous vesicular structures in the cytoplasm.The vesicular structures are released into the vacuolar space.The whole process is accompanied by disintegration of cytoplasm.Apparently isolated masses of cytoplasm occur in the luminaof laticifer tips in sections taken from dormant apices. Itis assumed that these masses have a role in the initiation ofnew laticifer regions in the next growing season. Ficus caricaL., laticifers, ultrastructure, development differentiation     

Role of arthropod communities in bioenergy crop litter decomposition†

The extensive land use conversion expected to occur to meet demands for bioenergy feedstock production will likely have widespread impacts on agroecosystem biodiversity and ecosystem services, including carbon sequestration. Although arthropod detritivores are known to contribute to litter decomposition and thus energy flow and nutrient cycling in many plant communities, their importance in bioenergy feedstock communities has not yet been assessed. We undertook an experimental study quantifying rates of litter mass loss and nutrient cycling in the presence and absence of these organisms in three bioenergy feedstock crops—miscanthus (Miscanthus x giganteus), switchgrass (Panicum virgatum), and a planted prairie community. Overall arthropod abundance and litter decomposition rates were similar in all three communities. Despite effective reduction of arthropods in experimental plots via insecticide application, litter decomposition rates, inorganic nitrogen leaching, and carbon–nitrogen ratios did not differ significantly between control (with arthropods) and treatment (without arthropods) plots in any of the three community types. Our findings suggest that changes in arthropod faunal composition associated with widespread adoption of bioenergy feedstock crops may not be associated with profoundly altered arthropod‐mediated litter decomposition and nutrient release.     

The influence of subepithelial connective tissues on epithelial proliferation in the adult mouse

Summary Subepithelial connective tissue is capable of modulating the pattern of histodifferentiation of stratified epithelia from adult animals, but it is not known whether the supporting connective tissue also influences epithelial proliferative activity. Epithelial and connective tissues of murine skin and oral mucosa, differing in their morphology and proliferative activity, were separated and heterotypically recombined prior to grafting to histocompatible hosts. After 3 or 8 weeks in situ, mitotic activity was determined following the administration of vinblastine sulfate. Although the mitotic activity in each of the epithelia could be modulated by some connective tissues, there was no distinct pattern of behavior. In combination with connective tissues from tongue or palate, the ear epidermis acquired a significantly increased mitotic activity. In contrast, when oral epithelia with high mitotic activity were recombined with dermal connective tissue, there was usually a significant reduction in proliferative activity. As there was no apparent association between mitotic activity and the induced changes in either organization or histodifferentiation, it is suggested that subepithelial connective tissue is capable of directly influencing the mitotic activity in the overlying epithelium.     

Effects of large herbivores on grassland arthropod diversity

Both arthropods and large grazing herbivores are important components and drivers of biodiversity in grassland ecosystems, but a synthesis of how arthropod diversity is affected by large herbivores has been largely missing. To fill this gap, we conducted a literature search, which yielded 141 studies on this topic of which 24 simultaneously investigated plant and arthropod diversity. Using the data from these 24 studies, we compared the responses of plant and arthropod diversity to an increase in grazing intensity. This quantitative assessment showed no overall significant effect of increasing grazing intensity on plant diversity, while arthropod diversity was generally negatively affected. To understand these negative effects, we explored the mechanisms by which large herbivores affect arthropod communities: direct effects, changes in vegetation structure, changes in plant community composition, changes in soil conditions, and cascading effects within the arthropod interaction web. We identify three main factors determining the effects of large herbivores on arthropod diversity: (i) unintentional predation and increased disturbance, (ii) decreases in total resource abundance for arthropods (biomass) and (iii) changes in plant diversity, vegetation structure and abiotic conditions. In general, heterogeneity in vegetation structure and abiotic conditions increases at intermediate grazing intensity, but declines at both low and high grazing intensity. We conclude that large herbivores can only increase arthropod diversity if they cause an increase in (a)biotic heterogeneity, and then only if this increase is large enough to compensate for the loss of total resource abundance and the increased mortality rate. This is expected to occur only at low herbivore densities or with spatio‐temporal variation in herbivore densities. As we demonstrate that arthropod diversity is often more negatively affected by grazing than plant diversity, we strongly recommend considering the specific requirements of arthropods when applying grazing management and to include arthropods in monitoring schemes. Conservation strategies aiming at maximizing heterogeneity, including regulation of herbivore densities (through human interventions or top‐down control), maintenance of different types of management in close proximity and rotational grazing regimes, are the most promising options to conserve arthropod diversity.