Barcoding Antarctic Biodiversity: current status and the CAML initiative,a case study of marine invertebrates

The Census of Antarctic Marine Life (CAML) aims to collate DNA barcode data for Antarctic marine species. DNA barcoding is a technique that uses a short gene sequence from a standardised region of the genome as a diagnostic ‘biomarker’ for species. This study aimed to quantify genetic data currently available in GenBank in order to establish whether a representative cross-section of Antarctic marine taxa and bio-geographic areas has been sequenced and to propose priorities for barcoding, with a particular emphasis on marine invertebrate species. It was found that, amongst marine invertebrate fauna, sequence information covers a limited range of taxa and areas—mainly Crustacea, Annelida and Mollusca from the Weddell Sea and the Antarctic Peninsula. Only 15% of genes sequenced in Antarctic marine invertebrates were the standard barcode gene cytochrome c oxidase subunit 1 (CO1), the majority were other nuclear and mitochondrial genes. There is an urgent need for more in-depth genetic barcoding and species identification studies in Antarctic science, from a range of taxa and areas, given the rate of climate-driven habitat changes that might lead to extinctions in the region. CAML hopes to redress the balance, by collecting and sequencing over the circum-Antarctic area, using material from voyages that occurred during 2008 and 2009, within the framework of the International Polar Year (IPY).     

Pathways of macroinvertebrate invasions in the Ob River basin (West Siberia)

Water bodies of West Siberia mainly belong to the Ob River basin, which is not connected to other basins by shipping canals. The relative isolation of the basin predetermined the major role of industrial fisheries and aquarium trade in alien invertebrate transfer into the basin reservoirs. About 60% of the alien species were introduced into water bodies of West Siberia through industrial fisheries, and about 40% through aquarium fisheries. This paper is the first attempt to supplement a list of alien aquatic invertebrates from the Ob River basin. The data on the spread of 21 known non-indigenous species of invertebrates in this area are available. It should be noted that 7 species were deliberately introduced to enhance food reserves for fish, 8 were released by aquarists, 5 were inadvertently released during fish and forage organism introduction, and 1 (a crayfish) was imported for human consumption. For species with a known establishment period, there was a prolonged lag time in cases of both intentional and inadvertent introduction. The high invasion rate in the relatively isolated water bodies of the Ob River basin is comparable to that in Europe; hence, establishment of control over fishery-induced movement of alien invertebrates is required.     

Crayfish invasion facilitates dispersal of plants and invertebrates by gulls

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Microfauna associated with algal mats in melt ponds of the Ross Ice Shelf

Summary The microfauna of benthic algal mats in eight ponds of diverse chemistry on the Ross Ice Shelf was examined. Tardigrades, nematodes and rotifers were successfully extracted from algal material by a modified Baermann funnel technique, which was robust enough to use under field conditions. Seven species of rotifer (of which 6 were bdelloids) and one species of nematode and tardigrade were found, all of which are cosmopolitan to Antarctic lentic ecosystems. Philodina sp. was the only invertebrate to occur in all ponds sampled. Rotifers were the most abundant invertebrates with average densities in all ponds of 4.26×10⁵ individuals/m², whereas nematodes were least abundant with densities of 4.96×10⁴ individuals/m². Total invertebrate densities and densities of individual taxa were significantly different in each of the 8 ponds, and of those measured environmental parameters were most strongly associated with conductivity. Cores taken from four ponds 2 cm into underlying substratum revealed that most animals live within the algal mats, with underlying sediment supporting a minimal population.     

An insect introduction to the maritime Antarctic

Although several invertebrates have been introduced by Man into the Antarctic, no holometabolous insects have survived to colonize terrestrial habitats successfully. Data are presented on the survival of populations of a chironomid midge, together with an enchytraeid worm, for 17 years in a maritime Antarctic site at Signy Island, South Orkney Islands. Both species are thought to have been introduced on plant material transplanted from either South Georgia or the Falkland Islands or both in 1967. Population densities average 25718m^-2 for the dipteran larvae and 3243 m^-2 for the worms. Successful completion of the midge's life cycle was indicated by emergence of brachypterous adults and oviposition (the population is parthenogenetic with only females present). Although both taxa are capable of supercooling to between -13 and -26°C, this capacity may not be sufficient in a severe winter to avoid lethal freezing. Four potential cryoprotectants were found in insect extracts, but in concentrations (< 1 % fresh weight) unlikely to influence cold hardiness. Both invertebrates appear to be pre-adapted for survival in much harsher conditions than they normally experience, by the extension of existing physiological mechanisms. It is concluded that the main limitations to invertebrate colonization of suitable Antarctic land areas by soil-dwelling species are geographical.     

Are Antarctic aquatic invertebrates hitchhiking on your footwear?

The increasing number of humans who travel to and within Antarctic regions each year not only increases the risk of introducing non-native species but also of translocating native species within and between Antarctic biogeoregions and poses the potential for artificial, human-mediated introduction of native freshwater invertebrate species to newly ice-free areas of Antarctica. This study was designed to test the potential for transfer of native Antarctic freshwater invertebrates and their cysts on footwear. An average of 1.86 Anostraca cysts, 29.47 Copepoda cysts, 4.29 Nematoda, 0.40 Rotifera and 0.966 Tardigrada individuals per gram of sediment were found in samples taken from footwear after contact with freshwater sediment. The invertebrate cysts isolated from the samples that underwent drying at 27 °C were able to hatch in tap water, and representatives of the other systematic groups (Nematoda, Rotifera, and Tardigrada) also remained viable.     

IACUC Challenges in Invertebrate Research

With billions of individuals and possibly hundreds of thousands of genera, invertebrates represent the largest number and greatest diversity of all animals used in research. Although the capacity for nociception is recognized in many invertebrate taxa, researchers and IACUC members are challenged by a lack of clear understanding of invertebrate welfare and by differing standards of moral concern for these taxa. In practice this has led IACUCs to consider invertebrates in two major groups: species worthy of increased moral concern approximating that shown to vertebrate species (this group includes cephalopods and to some extent decapod crustaceans) and all others. This dichotomy has led to differences in how invertebrate research is regulated and documented. This article presents two case studies illustrating specific concerns in invertebrate research protocols and then provides relevant information to address practical IACUC matters related to regulatory and ethical issues, sourcing and record keeping, risk management, assessment of pain and nociception in invertebrates, housing and husbandry, invasive procedures, veterinary care, and humane endpoints.     

Alien lichens unintentionally transported to the “Arctowski” station (South Shetlands, Antarctica)

The recent climate changes combined with intensified human activity in Antarctica are promoting the synanthropization process and increasing the likelihood of alien species establishing in the native communities. Cargo items, expedition members’ equipment and food destined for the 32nd Polish Antarctic Expedition to the “Arctowski” station in the 2007/2008 season were inspected to determine their potential as vectors for alien lichen species. Within the cargo, packaging and foodstuffs scanned, a total of 45 lichen specimens (24 species) were identified. Most of them had been accidentally transported with various timbers. Cargo containers and fresh food were also found to harbour for single specimens. The majority of lichens detected are alien to the Antarctic biota and had never been observed in the region. This paper estimates the potential risk of these lichens establishing themselves in remote southern latitudes. The results emphasize the threat of accidental introduction of alien organisms into Antarctica and the need for taking every precaution to prevent the importation of non-native species to this unique environment.     

Diaspores and phyto-remains accidentally transported to the Antarctic Station during three expeditions

The aim of the project was to assess the size and species range of alien plant diaspores and phyto-remains transported into the Polish Antarctic Station during three Antarctic expeditions. Our study clearly demonstrates that many diaspores can be quite easily unintentionally transported in good conditions to the Antarctic. In the analyzed material there were present diaspores of invasive species. All identified species belong to 20 families. The most abundant were Asteraceae and Poaceae species. The most interesting finding was the presence of caryopses of Poa annua, the first alien angiosperm species which already established a stable breeding population in the Antarctic. Base on our results, we can predict that risk of establishment of anther alien plant species in the vicinity of “Arctowski” Station is very high.     

Intentionally introduced terrestrial invertebrates: patterns,risks, and options for management

Our understanding and management of pathways of alien species introductions has improved significantly in the past few years. However, little attention has been paid in most parts of the world to the risks posed by the intentional introduction of alien terrestrial invertebrates which are not intended for use in biological control. We review the species and pathways involved in this intentional trade, and discuss key factors that mediate different aspects of risk. A total of 20 different intentions for the introduction of terrestrial invertebrates were identified. Uses and trade patterns have changed over time and further changes are likely in the future. In particular, invertebrates used in the pet trade, and as human food and animal feed are likely to increase in relevance. We assess priorities for future research and regulation based on the perceived “risk” of the uses including propagule pressure, security of captivity and ease of regulation. Regarding risk assessment, we examine three options: (a) using an existing generic protocol developed for a broad range of taxa; (b) developing a new protocol, possibly by adapting a protocol developed for other taxa; and (c) adopting the approach applied for biological control, i.e. structured experiments and observations. This review highlights the diversity of uses and associated threats of intentional terrestrial invertebrate introductions. It provides recommendations on how to tackle and prevent related issues and can therefore serve as a guideline for future work. We argue that the most suitable option for risk assessment might depend on the type or organism and the level of knowledge of the organism, as well as the intended use.     

Conservation of Southern Ocean Islands: invertebrates as exemplars

The Southern Ocean Islands (SOI) have an exceptionally high conservation status, and human activity on the islands is low by comparison with more tropical islands. In consequence, overexploitation, pollution and habitat destruction have had little influence on the invertebrate biotas of the islands, although overexploitation of pelagic species has the potential for an indirect influence via reduction of nutrient inputs to the terrestrial systems. By contrast, invasive alien species, the local effects of global climate change, and interactions between them are having large impacts on invertebrate populations and, as a consequence, on ecosystem functioning. Climate change is not only having direct impacts on indigenous invertebrates, but also seems to be promoting the ease of establishment of new alien invertebrate species. It is also contributing to population increases of invertebrate alien species already on the islands, sometimes with pronounced negative consequences for indigenous species and ecosystem functioning. Moreover, alien plants and mammals are also affecting indigenous invertebrate populations, often with climate change expected to exacerbate the impacts. Although the conservation requirements are reasonably well-understood for terrestrial systems, knowledge of freshwater and marine near-shore systems is inadequate. Nonetheless, what is known for terrestrial, freshwater and marine systems suggests that ongoing conservation of SOI invertebrates requires intervention from the highest political levels internationally, to slow climate change, to local improvements of quarantine measures to reduce the rates and impacts of biological invasions.     

Surviving out in the cold: Antarctic endemic invertebrates and their refugia

Aim To identify Antarctic palaeoendemic taxa and their probable glacial refugia from regional groups of endemic species records. Location Antarctica. Methods We compiled a list of Antarctic non‐marine invertebrates from published literature, and then deleted all records relating to non‐endemic, zoochoric (phoretic and parasitic), marine and partially identified species to leave only the elements endemic to Antarctica. We then used cluster analysis and principal components analysis to identify regional groupings within this endemic fauna. Results Some 170+ of the reported 520+ Antarctic invertebrates are free‐living and endemic, but only nine of these are pan‐Antarctic, with the majority having either ‘continental’/eastern or ‘maritime’/western distributions. Main conclusions All invertebrates endemic to continental Antarctica are confined to, or found adjacent to, ice‐free palaeorefugial mountains, nunataks and coastal exposures. By contrast, only one maritime Antarctic palaeorefugium has been identified, and most endemic taxa are currently associated with coastal lowland neorefugia. We suggest which regions of Antarctica (1) are likely to be refugial, and (2) simply require more data in order that the nature and origin of their fauna can be elucidated.     

Invertebrates in the canopy of tropical rain forests How much do we really know?

The current state of knowledge of canopy invertebrates in tropical rain forests is reviewed using data drawn, without bias toward taxon, collecting method or biogeographical region, from 89 studies concerned with mass-collecting (>1000 individuals). The review is intended to identify the most serious gaps and biases in the distribution of higher taxa among forest types and biogeographical regions. With respect to knowledge, biogeographical regions can be ranked as Neotropical > Australian > Oriental > Afrotropical. The canopy of lowland wet and subtropical forests has been studied in greater detail, whereas the canopy of lowland dry and montane forests is much less well known. Collecting techniques influence greatly the present knowledge of canopy invertebrates. Invertebrates other than arthropods, often abundant in epiphytic habitats, phytotelmata and perched litter, are virtually unknown. The abundance of several groups, such as Acari, Collembola and Isoptera, is almost certainly seriously underestimated. Densities of invertebrate individuals in the canopy of tropical rain forests appear to be lower than in temperate forests, although invertebrate abundance is dissipated by the high standing-biomass of rain forests. Coleoptera, particularly Staphylinidae, Curculionidae and Chrysomelidae, along with Hymenoptera, Lepidoptera and Araneae appear to be the most speciose taxa in the canopy, and it is probable that this reflects their range of feeding habits and exploitation of rain forests habitats. The distribution of individuals among the major arthropod orders and across the studies examined is complex and depends on many factors. The amount of variance that can be directly explained by biogeography, forest types (subtropical, wet, dry or montane), or collecting methods appears to be about 11%. The explained variance increases when considering major families of Coleoptera (28%) or subfamilies of Chrysomelidae (40%). In all cases, the variance explained by the type of forest is much higher than by that explained by biogeography. These conclusions are similar when considering various prey-predator relationships in the canopy. This suggests that, at the higher taxa level, the composition of the invertebrate fauna in the canopy may vary comparatively more across forest types than across biogeographical regions and this is discussed briefly from a conservation viewpoint.     

Invertebrate diversity on

Despite the global importance of New Zealands invertebrates, relatively little is known about them and their relationships with plants and plant communities in native habitats. Invertebrate diversity was examined by beating randomly chosen shrubs of the species Olearia bullata (Asteraceae) and Coprosma propinqua(Rubiaceae). Invertebrate taxon richness was assessed initially using morphospecies, which were identified subsequently by expert taxonomists. Though the taxon richness of invertebrates recorded from O. bullata was not significantly higher than that on C. propinqua (except for the orders Diptera and Hemiptera), there was a clear indication that O. bullata hosts a higher diversity of invertebrates. Mean number of taxa per shrub for O. bullata was higher in all cases (except Coleoptera), and so was the maximum number of taxa per shrub. Overall, O. bullata yielded 115 invertebrate taxa compared with 93 for C. propinqua. Moreover, 50 invertebrate taxa were restricted to O. bullata compared with 28 for C. propinqua. Since at least ten species of Oleariaare threatened or uncommon, this could be cause for concern with respect to the maintenance of invertebrate diversity. Therefore, sites where Oleariaspecies are still present are likely to be of significance for invertebrate conservation.     

Effect of alien riparian vegetation and its removal on a highly endemic river macroinvertebrate community

Invasive alien trees along river banks can reduce indigenous biodiversity, while their removal can restore it. We assessed here family- and species-level responses of river benthic macroinvertebrate assemblages to three riparian vegetation types (natural, alien trees, cleared of alien trees) in the Cape Floristic Region biodiversity hotspot. High species beta diversity of this highly endemic fauna meant that between-river, as well as seasonal effects, dominated assemblage patterns. SASS5, a qualitative, rapid bioassessment technique, based on the sensitivity of the families present, was used as a measure of river health and, indirectly, of water quality. SASS indicated a decline in water quality conditions after alien clearing, a likely response to the greater insolation and apparent erosion of cleared banks, resulting in elevated temperatures and suspended solids and lowered oxygen levels. Overall, cleared and natural sites were more similar to each other than to alien sites, suggesting some post-clearing recovery. However, many sensitive, endemic taxa survived in alien-invaded sites, and more than in the natural sites. These endemic species made use of shady, cool, high-oxygen levels under the alien tree canopy. However, endemics declined in overall abundance in sites cleared of aliens, being replaced by more tolerant, widespread taxa. Clearance of the alien trees opened up the rivers to sunny conditions, which had a major impact on community composition. Vegetation types, oxygen levels and river width were important environmental variables affecting these macroinvertebrate responses. Re-establishment of invertebrate biodiversity matched that of indigenous vegetation, with the most sensitive endemic taxa only recovering after establishment of bushy indigenous and shade-producing fynbos. Therefore, for biodiversity conservation objectives to be achieved, it is essential that indigenous plants are maintained and encouraged during and after clearing to ensure the recovery of endemic and sensitive taxa.     

Persistence and colonization strategies of playa wetland invertebrates

Wetland invertebrates have evolved numerous means of inhabiting spatially and temporally flooded wetland environments. The ability of invertebrates to either colonize from other sources and/or to persist in dry wetlands through diapause has seldom been simultaneously studied. We compared strategies of colonization and persistence by invertebrates in variable environments (playa wetlands on the Southern High Plains of Texas). We also examined emergence response time, following flooding, of taxa that persist in playa soil using field experiments and microcosms. At least 26 of 87 invertebrate taxa survive seasonal drying of playas through aestivation in soil. More invertebrate taxa only colonized flooded playas (70.1%) than only persisted in dry soil (29.9%) (P < 0.05). Of the invertebrate taxa that persisted in dry soil, more (P < 0.05) of these were active colonists or relied strictly on diapause rather than a combination of aestivation and colonization. Invertebrate densities were not statistically different among taxa that practiced colonization and persistence (5.2 invertebrates/m², SE = 2.0) or that only persisted (1.5 invertebrates/m², SE = 0.5) in playas (P=0.918). The average amount of time for a taxon to first appear in a microcosm was about 3 weeks less in 1995–96 than 1994–95, which was likely due to greater precipitation during 1995–96. We found that both colonization and persistence was practiced more often than a single strategy for those invertebrates sampled in microcosms. Conservation efforts for playa invertebrates should be implemented at the landscape level and focus on playas with intact watersheds, because these playas have relatively undisturbed hydroperiods.     

Long‐term patterns of invertebrate abundance and relationships to environmental factors in arid Australia

Resource pulses are a key feature of semi‐arid and arid ecosystems and are generally triggered by rainfall. While rainfall is an acknowledged driver of the abundance and distribution of larger animals, little is known about how invertebrate communities respond to rain events or to vegetative productivity. Here we investigate Ordinal‐level patterns and drivers of ground‐dwelling invertebrate abundance across 6 years of sampling in the Simpson Desert, central Australia. Between February 1999 and February 2005, a total of 174 381 invertebrates were sampled from 32 Orders. Ants were the most abundant taxon, comprising 83% of all invertebrates captured, while Collembola at 10.3% of total captures were a distant second over this period. Temporal patterns of the six invertebrate taxa specifically analysed (Acarina, ants, Araneae, Coleoptera, Collembola and Thysanura) were dynamic over the sampling period, and patterns of abundance were taxon‐specific. Analyses indicate that all six taxa showed a positive relationship with the cover of non‐Triodia vegetation. Other indicators of vegetative productivity (seeding and flowering) also showed positive relationships with certain taxa. Although the influence of rainfall was taxon‐dependent, no taxon was affected by short‐term rainfall (up to 18 days prior to survey). The abundance of Acarina, ants, and Coleoptera increased with greater long‐term rainfall (up to 18 months prior to survey), whilst Araneae showed the opposite effect. Temperature and dune zone (dune crest vs. swale) also had taxon‐specific effects. These results show that invertebrates in arid ecosystems are influenced by a variety of abiotic factors, at multiple scales, and that responses to rainfall are not as strong or as predictable as those seen for other taxa. Our results highlight the diversity of invertebrates in our study region and emphasize the need for targeted long‐term sampling to enhance our understanding of the ecology of these taxa and the role they play in arid ecosystems.     

Coral reef invertebrate microbiomes correlate with the presence of photosymbionts

Coral reefs provide habitat for an array of marine invertebrates that host symbiotic microbiomes. Photosynthetic symbionts including Symbiodinium dinoflagellates and diatoms potentially influence the diversity of their host-associated microbiomes by releasing carbon-containing photosynthates and other organic compounds that fuel microbial metabolism. Here we used 16S ribosomal RNA (rRNA) gene amplicon pyrosequencing to characterise the microbiomes of 11 common Great Barrier Reef marine invertebrate species that host photosynthetic symbionts and five taxa in which they are absent. The presence of photosynthetic symbionts influenced the composition but not the species richness, evenness and phylogenetic diversity of invertebrate-associated microbiomes. Invertebrates without photosynthetic symbionts were dominated by Alphaproteobacteria, whereas those hosting photosynthetic symbionts were dominated by Gammaproteobacteria. Interestingly, many microbial species from photosymbiont-bearing invertebrates, including Oceanospirillales spp., Alteromonas spp., Pseudomonas spp., Halomonas spp., are implicated in the metabolism of dimethylsulfoniopropionate (DMSP). DMSP is produced in high concentrations by photosynthetic dinoflagellates and is involved in climate regulation by facilitating cloud formation. Microbiomes correlated with host taxa and replicate individuals from most sampled species grouped in distance-based redundancy analysis of retrieved 16S rRNA gene sequences. This study highlights the complex nature of invertebrate holobionts and confirms the importance of photosynthetic symbionts in structuring marine invertebrate bacterial communities.