Tardigrades in the city: A review of diversity patterns in response to urbanization

In different taxonomical groups, the number of species found in urban environments tends to decline compared to adjacent nonurban environments. It is unclear whether tardigrades also conform to this pattern of diversity decline in cities. Tardigrades are microscopic invertebrates which have been understudied, despite the fact that they are cosmopolitan and found in all types of habitats. Due to their capability to withstand extreme conditions, tardigrades should be able to successfully thrive in urban environments. Here, all available information about tardigrade diversity in cities was compiled. It was quantitatively determined that tardigrade diversity declines in urban areas compared to adjacent rural areas. Geographically, closer cities are also likely to harbor a more similar set of tardigrade species. In comparison to other groups like mammals and birds, there are no tardigrade species consistently found in most studied cities. In fact, most urban tardigrades have only been found in one single city. Ultimately, the species of tardigrades found in a given city will normally depend on the set of species already living in the adjacent native environments. One question that deserves further investigation is why only a subset of such native species is able to colonize the new environmental niches available in cities

Tardigrade Abundance in Relation to Urbanisation and Highly Anthropogenic Substrates

Animals colonising urban environments are exposed to a series of novel stressors and ecological challenges, which can result in adaptations to alternative urban niches. Tardigrades are cosmopolitan invertebrates present in all types of ecosystems, including urban environments; and they can survive under extreme conditions, including periods of desiccation, thus allowing them to colonise novel harsh habitats. Tardigrades are thus a promising model to investigate the challenges and opportunities encountered by urban colonisers. Our aims were 1, to determine if tardigrade abundance in natural substrates (moss, lichen and leaf litter) differs between rural and urban sites and 2, to assess if tardigrades have successfully colonised urban substrates that are highly anthropogenic (road sediment, and material accumulated under cars and in wall crevices). Among natural substrates, we found fewer tardigrades in Cork city than in rural sites. However, in urban sites we found no differences between the number of tardigrades present in natural and anthropogenic substrates. In fact, the highest tardigrade abundances in urban samples were found in abiotic material accumulated in wall crevices. We conclude that even though urbanisation may restrict tardigrade abundance, this group of organisms can successfully colonise alternative urban substrates. More research is needed on the ability of tardigrades and other taxa to inhabit highly unusual and disturbed urban substrates effectively, and the adaptations that may take place when animals colonise such substrates

Importance of Taxonomic Group, Life Stage and Circumstance of Rescue upon Wildlife Rehabilitation in Ontario, Canada

Wildlife rehabilitation is an increasingly important and global practice, aiming towards advancements in animal welfare and species conservation. Although there are ongoing discussions on the benefits and limitations of wildlife rehabilitation, there is a general agreement on the importance of wildlife rehabilitation on improving the welfare of wild animals and identifying threats to wildlife. Determining which factors lead to a successful outcome of rehabilitation can allow wildlife rehabilitation centres to best focus their resources to benefit animals with the greatest chance of a successful release. In this study, three factors affecting the success of rehabilitation were evaluated: taxonomic group, life stage and circumstance of rescue. We used a large database of patients’ records (9561 animals from 198 species) from Sandy Pines Wildlife Centre (Ontario, Canada) over a three year study period (from 2015 to 2018). We found that reptiles had a higher rate of release (63.6 %), compared with mammals (42.1 %) and birds (48.3 %), although released reptiles spent longer in the centre than birds and mammals. Animals arriving to the centre in poor condition were less likely to be rehabilitated and spent longer in the centre than animals arriving in good condition. Overall, preadults were more likely to be released than adults, although the number of days spent at the centre did not differ by life stage. Animals suffering active damage (e.g. ‘collision’ and ‘projectile’) were less likely to be rehabilitated than animals suffering passive damage (e.g. arriving to the centre as ‘orphan’ or due to ‘habitat destruction’); however, when only considering those animals that left the centre, the number of days spent at the centre did not differ between animals suffering passive or active damage. The analysis of patients’ records can provide relevant information to rehabilitators about factors influencing rehabilitation efforts, which can be used to implement strategies that maximise release rates, given limited resources

Changes in the Home Range Sizes of Terrestrial Vertebrates in Response to Urban Disturbance: A Meta-Analysis

The unprecedented growth rate in human population and the increasing movement of people to urban areas is causing a rapid increase in urbanisation globally. Urban environments may restrict or affect the behaviour of many animal species. Importantly, urban populations may change their spatial movement, particularly decreasing their home ranges in response to habitat fragmentation, the presence of landscape barriers and the availability and density of resources. Several species specific studies suggest that urban animals decrease their home ranges compared with their non-urban counterparts; however, it remained unclear whether this pattern is widespread across taxa or is instead restricted to specific taxonomic groups. Consequently, we conducted a meta-analysis, collecting 41 sets of data comparing home ranges in both natural and urban environments in 32 species of reptiles, birds and mammals. We calculated effect sizes as the difference in animal home range sizes between natural and urban environments. We found that the home ranges were smaller in urban environments compared with natural environments (mean effect size = -0.844), and we observed a similar result when considering birds and mammals separately. We also found that home range sizes were not significantly affected when disturbance in urban areas was minimal, which suggests that many species may be able to tolerate low levels of disturbance without changing their movement patterns. Our study thus indicates that increasing levels of urbanisation restrict the spatial movement of species across taxa; this information is relevant for ecological studies of further urban species as well as for the development of management strategies for urban populations

Shyer and larger bird species show more reduced fear of humans when living in urban environments

As the natural habitats of many species are degraded or disappear, there is scope for these species to be established in urban habitats. To ease the establishment and maintenance of urban populations of more species we need to better understand what degree of phenotypical change to expect as different species transition into urban environments. During the first stages of urban colonization, behavioural changes such as an increase in boldness are particularly important. A consistent response in urban populations is to decrease the distance at which individuals flee from an approaching human (flight initiation distance, or FID). Performing a phylogenetic generalized least-squares (PGLS) analysis on 130 avian species, I found that the largest changes in FID between rural and urban populations occur in species that are larger-bodied and naturally shy (higher rural FID), two phenotypic traits that are not normally associated with urban colonizers. More unlikely species may thus be able to colonize urban environments, especially if we design cities in ways that promote such urban colonizations

Not all cities are the same: variation in animal phenotypes across cities within urban ecology studies

The sustained expansion of urban environments has been paralleled by an increase in the number of studies investigating the phenotypic changes of animals driven by urbanization. Most of these studies have been confined to only one urban center. However, as the types and strength of anthropogenic stressors differ across cities, a generalizable understanding of the effects of urbanization on urban-dwelling species can only be reached by comparing the responses of urban populations from the same species across more than one city. We conducted phylogenetic meta-analyses on data for animal species (including both invertebrates and vertebrates) for which measures about any morphological, physiological, or behavioral trait were reported for two or more cities. We found that morphological, physiological and behavioral traits of urban animals all differ similarly across cities, and that such phenotypic differences across cities increase as the more cities were investigated in any given study. We also found support for phenotypic differences across cities being more pronounced as the farther away cities are from each other. Our results clearly indicate that separate urban populations of the same species can diverge phenotypically, and support previous pleas from many researchers to conduct urban studies across several urban populations. We particularly recommend that future studies choose cities in different biomes, as urban adaptations may differ substantially in cities sited in different ecological matrices. Ultimately, a generalized knowledge about how organisms are affected by urbanization will only be possible when comprehensive biological patterns are similarly studied across separate and distinct cities

Effects of metabolic rate and sperm competition on the fatty-acid composition of mammalian sperm

The sperm membrane is a key structure affecting sperm function and thus reproductive success. Spermatozoa are highly specialized and differentiated cells that undergo a long series of processes in the male and female reproductive tracts until they reach the site of fertilization. During this transit, the sperm membrane is prone to damage such as lipid peroxidation. The characteristics and performance of the sperm membrane are strongly determined by the fatty-acid composition of membrane phospholipids. Polyunsaturated fatty-acids (PUFAs) are the most prone to lipid peroxidation. Lipid peroxidation and other types of oxidative damage increase with higher metabolism and with higher levels of sperm competition due to the increased ATP production to fuel higher sperm velocities. Consequently, we hypothesized that, in order to avoid oxidative damage, and the ensuing impairment of sperm function, sperm cells exhibit a negative relationship between PUFA content and mass-specific metabolic rate (MSMR). We also hypothesized that higher sperm competition leads to a reduction in the proportion of sperm PUFAs. We performed a comparative study in mammals and found that high MSMR and high levels of sperm competition both promote a decrease in the proportion of PUFAs that are more prone to lipid peroxidation. The negative relationship between MSMR and these PUFAs in sperm cells is surprising, because a positive relationship is found in all other cell types so far investigated. Our results support the idea that the effects of MSMR and sperm competition on sperm function can operate at very different levels. © 2013 European Society For Evolutionary Biology.This work was supported by a Ramón y Cajal fellowship (RYC-2011-07943) to J.d.-T. and grants from the Spanish Ministry of Economy and Competitiveness (CGL2011-26341 to E.R.S.R. and CGL2012-37423 to J.d.-T.).Peer Reviewe

Is male reproductive senescence minimised in Mus species with high levels of sperm competition?

Sperm competition, an evolutionary process in which the spermatozoa of two or more males compete for the fertilization of the same ovum, gives rise to several morphological and physiological adaptations. Generally, high levels of sperm competition enhance sperm function. In contrast, advanced age is known to lead to reproductive senescence, including a general decline in sperm function. Sperm competition and advanced age may thus have opposing effects on sperm function. Here, we tested the hypothesis that the increase in sperm function in species experiencing high levels of sperm competition will counteract the negative effects of advanced age. We measured a comprehensive set of reproductive traits in young and old males in three species of mice of the genus Mus, which differ greatly in their levels of sperm competition. Our prediction was that the expression of reproductive senescence would be highest in the species with low levels of sperm competition and lowest in the species with high levels of sperm competition. Surprisingly, we did not find a strong signal of reproductive senescence in any of the three Mus species. Overall, our results did not clearly support our hypothesis that high levels of sperm competition minimize the negative effects of ageing on sperm function

A cost for high levels of sperm competition in rodents: Increased sperm DNA fragmentation

Spermcompetition, a prevalent evolutionary process inwhich the spermatozoa of two or more males compete for the fertilization of the same ovum, leads to morphological and physiological adaptations, including increases in energetic metabolism that may serve to propel sperm faster but that may have negative effects onDNA integrity. SpermDNA damage is associated with reduced rates of fertilization, embryo and fetal loss, offspring mortality, and mutations leading to genetic disease. We tested whether high levels of sperm competition affect sperm DNA integrity. We evaluated sperm DNA integrity in 18 species of rodents that differ in their levels of spermcompetition using the spermchromatin structure assay. DNA integrity was assessed upon sperm collection, in response to incubation under capacitating or non-capacitating conditions, and after exposure to physical and chemical stressors. Sperm DNA was very resistant to physical and chemical stressors, whereas incubation in noncapacitating and capacitating conditions resulted in only a small increase in spermDNA damage. Importantly, levels of spermcompetition were positively associated with sperm DNA fragmentation across rodent species. This is the first evidence showing that high levels of sperm competition lead to an important cost in the form of increased sperm DNA damage.Peer Reviewe

Metabolic rate limits the effect of sperm competition on mammalian spermatogenesis.

Sperm competition leads to increased sperm production in many taxa. This response may result from increases in testes size, changes in testicular architecture or changes in the kinetics of spermatogenesis, but the impact of each one of these processes on sperm production has not been studied in an integrated manner. Furthermore, such response may be limited in species with low mass-specific metabolic rate (MSMR), i.e., large-bodied species, because they cannot process energy and resources efficiently enough both at the organismic and cellular levels. Here we compare 99 mammalian species and show that higher levels of sperm competition correlated with a) higher proportions of seminiferous tubules, b) shorter seminiferous epithelium cycle lengths (SECL) which reduce the time required to produce sperm, and c) higher efficiencies of Sertoli cells (involved in sperm maturation). These responses to sperm competition, in turn, result in higher daily sperm production, more sperm stored in the epididymides, and more sperm in the ejaculate. However, the two processes that require processing resources at faster rates (SECL and efficiency of Sertoli cells) only respond to sperm competition in species with high MSMR. Thus, increases in sperm production with intense sperm competition occur via a complex network of mechanisms, but some are constrained by MSMR