Urban soil quality deteriorates even with low heavy metal levels: An arthropod-based multi-indices approach.

Urban-induced habitat conversion drastically changes soil life in a variety of ways. Soil sealing, human disturbance, habitat fragmentation, industrial and vehicular pollution are the main causes of urban soil degradation. Soil arthropods, as one of the most abundant and diverse group of soil fauna, are involved in many soil processes that are of great importance in maintaining soil health and multifunctionality. Nevertheless, soil quality is still mainly characterized by physical, chemical, and microbiological parameters. Here, we assessed and compared the biological soil quality in woody (REF: reference forest, REM: remnant forest) and nonwoody (TURF: public turfgrass, and RUD: ruderal habitat) types of urban green spaces along a disturbance and management intensity gradient in the Budapest metropolitan area (Hungary), using community metrics and soil arthropod-based indicators. Vegetation cover and landscape characteristics of study sites were quantified through vegetation and urbanization indices, respectively. Basic soil properties, total and bioavailable concentrations of the main heavy metals (Cd, Co, Hg, Ni, Zn) were also measured. Acari, Collembola, and Hymenoptera (mainly Formicidae) were the most abundant groups. Litter-dweller taxa, particularly Protura, proved to be the most sensitive to urban disturbance. Representatives of Hemiptera, Diptera, Symphyla, and Pauropoda were common in low densities. The taxonomic diversity of soil arthropod assemblages in nonwoody and woody habitats was similar. Although the integrated faunal indices showed no differences among soil habitat types, they provided different responses and, consequently, different information. Our findings demonstrated that the biological quality and arthropod community structure of soils were strongly impacted by soil C/N and heavy metal contamination. We found that low and moderate levels of pollution have adverse effects on edaphic fauna, suggesting biological degradation of soils, even below pollution limits. Nevertheless, more disturbed urban green spaces have been shown to play a significant role in maintaining belowground biodiversity, thereby soil functions.

Urban effects on saprophagous macroarthropods are mainly driven by climate: A global meta-analysis.

Macrodecomposers provide important ecosystem services even in human dominated habitats including urban ecosystems, but the effect of urban land conversion on their species diversity and abundance has not been explored at global scale. Here, we present the first meta-analysis to quantify the general response of two major arthropod taxa, terrestrial isopods and millipedes to urbanization and to reveal the underlying mechanisms. Climatic (temperature, precipitation, growing season length), edaphic (pH, organic carbon, CaCO3 and clay content of surface soils), urban (population density, city age, vegetation cover and mean actual evapotranspiration) parameters and methods of study (duration, sampling technique, replications) were used as moderators. We used a hierarchical meta-analytic approach to consider the dependence of multiple effect sizes obtained from one study. Altogether 156 paired observations were extracted from 59 urban studies conducted between 1980 and 2020. Urbanization had a negative effect on species diversity (species richness and Shannon index) of both macroarthropod taxa. However, both the direction and strength of their abundance response varied to a greater extent, resulting in a neutral effect of urban disturbance on them. The key drivers influencing the urban effects on macroarthropods were mean annual temperature and precipitation, absolute minimum temperature and length of growing season. The study also highlighted the importance of sampling methods: direct sampling (hand collecting) resulted in stronger urban effects presumably due to several sources of sampling bias. Our global synthesis highlighted that urbanization is a threat to soil arthropods, particularly to litter-dwelling detritivores, which potentially alters plant residue processing and ultimately soil biogeochemical cycles.

Taxi drivers: the role of animals in transporting mycorrhizal fungi.

Dispersal of mycorrhizal fungi via animals and the importance for the interacting partners' life history as well as for ecosystems is an understudied topic. In this review, we describe the available evidence and the most important knowledge gaps and finally suggest ways to gain the missing information. So far, 33 articles have been published proving a successful transfer of mycorrhizal propagules by animals. The vast majority of research on invertebrates was focused on arbuscular mycorrhizal (AM) fungi, whereas papers on vertebrates (mainly rodents and artiodactyls) equally addressed ectomycorrhizal (ECM) and AM fungi. Effective dispersal has been mostly shown by the successful inoculation of bait plants and less commonly by spore staining or germination tests. Based on the available data and general knowledge on animal lifestyles, collembolans and oribatid mites may be important in transporting ECM fungal propagules by ectozoochory, whereas earthworms, isopods, and millipedes could mainly transfer AM fungal spores in their gut systems. ECM fungal distribution may be affected by mycophagous dipterans and their hymenopteran parasitoids, while slugs, snails, and beetles could transport both mycorrhizal groups. Vertebrates feeding on fruit bodies were shown to disperse mainly ECM fungi, while AM fungi are transported mostly accidentally by herbivores. The important knowledge gaps include insufficient information on dispersal of fungal propagules other than spores, the role of invertebrates in the dispersal of mycorrhizal fungi, the way in which propagules pass through food webs, and the spatial distances reached by different dispersal mechanisms both horizontally and vertically.

Taxonomic and Functional Response of Millipedes (Diplopoda) to Urban Soil Disturbance in a Metropolitan Area.

Urbanization, as a major cause of local species extinction and biotic homogenization, drastically alters soil life. Millipedes are a key group of soil macrodetritivores and significantly influence soil quality, mainly through their essential role in nutrient cycling. Therefore, studying their taxonomic and functional responses to urban disturbance is crucial, as they contribute to the provision of several soil-related ecosystem services in cities. Differently degraded rural, urban forests and other woody patches (e.g., parks, gardens, and cemeteries) were sampled on Buda and Pest sides of the Budapest metropolitan area divided by the Danube River. We measured the most relevant physical and chemical properties of topsoil to characterize habitats. We applied an urbanization index based on vegetation cover and built-up area of the study sites to quantify urban intensity. The composition of the assemblages was determined by the division of the city along the Danube. Urbanization was associated with a reduction in species and functional richness of millipedes on both sides of Budapest. ß diversity and species turnover increased with urban intensity. Urban disturbance was the main driver in assembly of taxonomic and functional community composition. A new species (Cylindroiulus caeruleocinctus (Wood, 1864)) to the fauna of Budapest was found. Detritivore invertebrates depend on leaf litter and other dead organic matter types, therefore microsites providing these resources greatly improve their survival. Due to increasing urban disturbance, it is recommended to provide appropriate detritus and shelter sites as part of the management of green spaces in order to maintain species richness, abundance, and function of species.

Isopod distribution and climate change.

The unique properties of terrestrial isopods regarding responses to limiting factors such as drought and temperature have led to interesting distributional patterns along climatic and other environmental gradients at both species and community level. This paper will focus on the exploration of isopod distributions in evaluating climate change effects on biodiversity at different scales, geographical regions, and environments, in view of isopods' tolerances to environmental factors, mostly humidity and temperature. Isopod distribution is tightly connected to available habitats and habitat features at a fine spatial scale, even though different species may exhibit a variety of responses to environmental heterogeneity, reflecting the large interspecific variation within the group. Furthermore, isopod distributions show some notable deviations from common global patterns, mainly as a result of their ecological features and evolutionary origins. Responses to human disturbance are not always traceable, but a trend towards community homogenisation is often found under strong global urbanisation processes. In general, even though it is still not clear how predicted climate change will affect isopod distribution, there is evidence that mixed effects are to be expected, depending on the region under study. We still lack robust and extensive analyses of isopod distributions at different scales and at different biomes, as well as applications of distribution models that might help evaluate future trends.

Terrestrial isopods in urban environments: an overview.

In an increasingly urbanized world scientific research has shifted towards the understanding of cities as unique ecosystems. Urban land use change results in rapid and drastic changes in physical and biological properties, including that of biodiversity and community composition. Soil biodiversity research often lags behind the more charismatic groups such as vertebrates and plants. This paper attempts to fill this gap and provides an overview on urban isopod research. First, a brief overview on urban land use change is given, specifically on the major alterations on surface soils. Historical studies on urban isopods is summarized, followed by the status of current knowledge on diversity, distribution, and function of urban isopod species and communities. A review of more than 100 publications revealed that worldwide 50 cities and towns have some record of terrestrial isopod species, but only a few of those are city-scale explorations of urban fauna. A total of 110 isopod species has been recorded although the majority of them only once. The ten most frequently occurring isopods are widely distributed synanthropic species. Knowledge gaps and future research needs call for a better global dataset, long term monitoring of urban populations, multi-scale analyses of landscape properties as potential drivers of isopod diversity, and molecular studies to detect evolutionary changes.

The role of urban forest patches in maintaining isopod diversity (Oniscidea).

Compositional changes in natural communities associated with anthropogenic influence often lead to localised extinctions and biodiversity loss. Soil invertebrates are also threatened by urbanisation due to habitat fragmentation, vegetation changes and management, soil alteration, degradation, and disappearing shelter sites. The aim was to assess terrestrial isopod (Oniscidea) assemblages in differently degraded urban forest patches of a metropolitan area (Budapest, Hungary). Study sites were compared by their species richness, composition and the relevant background factors (soil properties, dead wood, litter characteristics, and canopy closure). The degree of urban disturbance was expressed using an urbanisation index (UI) based on built-up density and vegetation cover. The isopods were identified to species level, and were qualified by their habitat preference and naturalness index (TINI). Average Rarity Index (ARI), derived from TINIs provided information on the degree of naturalness/disturbance of each habitat. Altogether 14 isopod species were collected from 23 sample sites. Urbanisation indirectly affected on the composition of isopod assemblages through the quantity of dead wood and soil plasticity. ARIs and UIs of sample sites were negatively correlated. Urban patches harboured habitat generalist, synanthropic and established introduced species with low naturalness value of assemblages. Areas with no or low anthropogenic disturbance maintained stable native, autochthonous assemblages that were characteristic of rural sites in the region. Transitional zones between rural and urban habitats usually maintained a mixed isopod fauna consisting of both urban and rural elements.

Life history characteristics of a cave isopod (Mesoniscusgraniger Friv.).

The special environmental conditions of caves provide habitat for several endemic and relict species, among them terrestrial isopods. The Baradla Cave system (north-eastern Hungary) hosts Mesoniscusgraniger (Frivaldszky, 1865) (Oniscidea, Microcheta, Mesoniscidae), a pygmy, blind, fragile troglophile woodlice species. Its stable environment can be characterised by the lack of light, high relative humidity (96%), low and constant temperature (about 10 °C). We explored the population characteristics (sex ratio, size distribution) and life history traits of the species (e.g. longevity, reproductive strategy, offspring number, and size). Sex ratio and size distribution of the individuals (head-width measurements) were estimated based on a yearly pooled pitfall-trap data set (N = 677). We studied the species' reproductive strategy under natural conditions (Baradla Cave, Aggtelek National Park). Model populations were set up in the cave and checked monthly between March and October, 2016 (15 replicates, each with 12 randomly chosen adult individuals; ΣN = 180). Digital photos were taken of the live animals and their length was estimated based on the photos by using ImageJ software (average body length: 6.56 ± 0.79 mm). The results showed female dominance in the population [(male:female = 0.43:0.57); p < 0.001 (GLM)]. Female head width (0.87 ± 0.18 mm) was significantly greater than that of males [0.79 ± 0.08 mm; p < 0.001 (t-test)]. Based on our present data we assume that the offspring number per single female is low (3-5), and new-borns have a relatively large size (body length: 4.22 ± 0.53 mm) compared to the adults. The probability of reproduction was continuous by monthly intervals (binomial test) and longevity exceeds one year. Our results suggest that the species follows a stenodynamic life history.

Morphological traits - desiccation resistance - habitat characteristics: a possible key for distribution in woodlice (Isopoda, Oniscidea).

Terrestrial isopods, as successful colonizers of land habitats, show a great variety in species distribution patterns on a global, continental, or regional scale. On a local, within-habitat level these patterns reflect the species' tolerance limits and the presence of suitable hiding places (shelter sites, refugia). Humidity preference reflects a species' capability for water retention which, in turn, depends on the integumental barrier. Desiccation resistance is a key feature in isopod survival under different environmental conditions. The present study shows a correlation between cuticle thickness and desiccation resistance under three relative humidity (RH) ranges (about 30, 75 and 100% RH) in nine species, relating these to the species' differences in meso- and microhabitat choices. Habitat preferences are also associated with differences in cuticle surface morphology. The results support our hypothesis that species distribution and desiccation resistance are associated with particular cuticular morphological traits. Phylogenetic relations seem to be less important in desiccation resistance than cuticle thickness and external morphology.

Histological studies on the marsupium of two terrestrial isopods (Crustacea, Isopoda, Oniscidea).

The marsupium, a brood pouch in peracarid crustaceans (Crustacea, Malacostraca) has evolved in terrestrial environment for providing nutrition and optimal conditions for embryogenesis. In the present study we give details on the histology and ultrastructure of its constituting elements such as oostegites and cotyledons. Marsupia of two different eco-morphological types of woodlice, namely the non-conglobating species Trachelipusrathkii Brandt, 1833 and the conglobating species Cylisticusconvexus De Geer, 1778 were investigated. Light microscopic (LM) studies showed some differences in the main structure of the two species' brood pouch: in Trachelipusrathkii, a 'clinger' type woodlice, the oostegites bend outwards during brood incubation as growing offspring require more space, while in Cylisticusconvexus, a 'roller' type isopod, the sternites arch into the body cavity to ensure space for developing offspring and still allowing conglobation of the gravid females. The quantitative analysis of the oostegites' cuticle proved that the outer part is about 2.5 - 3 times thicker compared to the inner part in both species. Electron microscopic (TEM) examinations show only small histological differences in the oostegites and cotyledon structure of the two species. Cellular elements and moderately electron dense fleecy precipitate are found in the hemolymph space between the two cuticles of oostegites. The cells contain PAS positive polysaccharide areas. TEM studies revealed some differences in the cotyledon ultrastructure of the two species. Cotyledons of Trachelipusrathkii consist of cells with cristate mitochondria and granular endoplasmic reticulum with cisterns. Cotyledons of Cylisticusconvexus consist of cells with densely cristate mitochondria and ribosomes attached to vesicular membrane structures. In both species cells with electron dense bodies were observed. We conclude that - besides the differences in marsupial shapes - the fine structure of the oostegites and cotyledons is hardly affected by the eco-morphological type, specifically the conglobating or non-conglobating character of the studied species.

Demography of some non-native isopods (Crustacea, Isopoda, Oniscidea) in a Mid-Atlantic forest, USA.

Introduced species dominate the terrestrial isopod fauna in most inland habitats of North America, including urban landscapes. These non-native species are often very abundant and thus potentially play a significant role in detritus processing. We monitored isopod assemblages in an urban forest for a year to examine the relationship between surface activity and abiotic environmental factors, and to analyze reproductive characteristics that might contribute to their successful establishment. Using pitfall trap samples we recorded five species, two of which, Trachelipusrathkii and Cylisticusconvexus, were highly abundant. We determined size, sex and reproductive state of each individual. Surface activity of both species reflected variability in abiotic stress factors for isopods, such as soil moisture and soil temperature. Early spring the main trigger was soil temperature while later in the season increasing temperature and decreasing soil moisture jointly affected population dynamics. Activity significantly correlated with soil moisture. The temporal pattern of sex ratios supported the secondary sex ratio hypothesis. Males dominated the samples on the onset of the mating season in search of females. The pattern was reversed as females searched for suitable microsites for their offspring. Size independent fecundity decreased as conditions became more stressful late in the season.

Eco-morphological studies on pleopodal lungs and cuticle in Armadillidium species (Crustacea, Isopoda, Oniscidea).

Terrestrial isopods (Crustacea, Isopoda, Oniscidea) have adapted to land life by diverse morphological, physiological and behavioral changes. Woodlice species exhibit a large variety in this respect, their preferences ranging from moist to dry habitats. These moisture preference values are related to various morphological adaptations, rendering terrestrial isopods amenable to studying morphological adaptations to terrestrial life. We performed a comparison of four Armadillidium species (Armadillidium zenckeri, Armadillidium nasatum, Armadillidium versicolor, Armadillidium vulgare), by quantifying two morphological traits: the extent of the interfacial endothelium between the respiratory space and the hemolymph within pleopodal lungs and the thickness of tergite cuticle, which are 'key factors' in determining protection from desiccation. These values were measured from light micrographs of cross-sectioned lungs. The cosmopolitan A. vulgare, as a habitat generalist, seems to be the most resistant against desiccation and other environmental conditions, while A. zenckeri is the most sensitive one. Light microscopic studies revealed that the four species can be ordered similarly, if we compare them by the extension of the endothelial interface and cuticle thickness, suggesting that these morphological traits are important determinants of their distribution on habitat, microhabitat scales and through the existence of suitable habitats - together with many other factors - the geographical pattern of species occurence.

Size dependent differences in litter consumption of isopods: preliminary results.

A series of experiments were applied to test how leaf orientation within microcosms affect consumption rates (Experiment 1), and to discover intra-specific differences in leaf litter consumption (Experiment 2) of the common isopod species Porcellio scaber and Porcellionides pruinosus. A standardised microcosm setup was developed for feeding experiments to maintain standard conditions. A constant amount of freshly fallen black poplar litter was provided to three distinct size class (small, medium, large) of woodlice. We measured litter consumption after a fortnight. We maintained appr. constant isopod biomass for all treatments, and equal densities within each size class. We hypothesized that different size classes differ in their litter consumption, therefore such differences should occur even within populations of the species. We also hypothesized a marked difference in consumption rates for different leaf orientation within microcosms. Our results showed size-specific consumption patterns for Porcellio scaber: small adults showed the highest consumption rates (i.e. litter mass loss / isopod biomass) in high density microcosms, while medium-sized adults of lower densities ate the most litter in containers. Leaf orientation posed no significant effect on litter consumption.