ITS, OTUs and beyond—fungal hyperdiversity calls for supplementary solutions

Molecular species recognition of fungi emerged years before DNA barcoding ( Seifert 2009 ). While the ideal fungal DNA barcode seems Utopian, two research decades nevertheless highlight the internal transcribed spacer (ITS) as the best available choice ( Seifert 2009 ). Databases providing reliable ITS sequences of known fungi require enormous efforts, but are urgently needed ( Abarenkov et al. 2010a,b ; Begerow et al. 2010 ). Any criticism of such a commitment seems unjustified. However, exclusive focus on the development of ITS reference libraries will delay the progress towards a deeper ecological insight. It is widely acknowledged that ITS fails to recognize species, particularly in some ascomycete lineages ( Balajee et al. 2009 ; Seifert 2009 ). It also appears paradoxical to solely rely on ITS for ecological recognition of fungal species when modern fungal systematics rely on phylogenetic species recognition with concordance of multiple gene genealogies (see Blackwell 2011 ). Considering that at least 98% of the predicted ～5 million fungal species remain undescribed ( Blackwell 2011 ), how will reliance on ITS alone influence the biodiversity estimates and ecological understanding? In this issue, Gazis et al. (2011) elegantly demonstrate through multi‐locus sequence phylogeny analyses that ITS largely underestimates the species diversity of tropical fungal endophytes and even more importantly obscures fundamental ecological and biogeographical patterns. This thorough reflection on species delimitation criteria and their implications for ecological and biogeographical inferences underline that ITS, particularly in hyperdiverse habitats, provides no shortcut to deeper knowledge of fungal ecology.     

Intergenerational reproductive parasitism in a stingless bee

Insect colonies have been traditionally regarded as closed societies comprised of completely sterile workers ruled over by a single once-mated queen. However, over the past 15 years, microsatellite studies of parentage have revealed that this perception is far from the truth ( Beekman & Oldroyd 2008 ). First, we learned that honey bee queens are far more promiscuous than we had previously imagined ( Estoup et al. 1994 ), with one Apis dorsata queen clocked at over 100 mates ( Wattanachaiyingcharoen et al. 2003 ). Then Oldroyd et al. (1994) reported a honey bee colony from Queensland, where virtually all the males were sons of a single patriline of workers – a clear case of a cheater mutant that promoted intra-colonial reproductive parasitism. Then we learned that both bumble bee colonies ( Lopez-Vaamonde et al. 2004 ) and queenless honey bee colonies ( Nanork et al. 2005, 2007 ) are routinely parasitized by workers from other nests that fly in and lay male-producing eggs that are then reared by the victim colony. There is even evidence that in a thelytokous honey bee population, workers lay female-destined eggs directly into queen cells, thus reincarnating themselves as a queen ( Jordan et al. 2008 ). And let us not forget ants, where microsatellite studies have revealed equally bizarre and totally unexpected phenomena (e.g. Cahan & Keller 2003 ; Pearcy et al. 2004 ; Fournier et al. 2005 ). Now, in this issue, Alves et al. (2009) use microsatellites to provide yet another shocking and completely unexpected revelation about the nefarious goings-on in insect colonies: intergenerational reproductive parasitism by stingless bee workers.     

How local extinction changes rarity: an example with Sonoran Desert fishes

That spatially rare species may be predisposed to extinction is a common tenet of ecology. However, the opposite side of the relationship – how extinction alters spatial rarity – remains little explored. We used an extensive biodiversity database to contrast patterns of spatial rarity of a biogeographic assemblage of native Sonoran fishes before and after an extensive, decades-long wave of extirpations. Focusing on 25 fish species native to the Lower Basin of the Colorado River, we analyzed two key aspects of spatial rarity: 1) species range sizes (expressed as kilometers of stream reach occupied) and 2) species' co-occurrence patterns. Native fish species that were spatially rare historically suffered disproportionate losses in occurrences. However, endemic species did not suffer increased losses relative to non-endemic (but still native) species of comparable rarity. Species' geographic range sizes were concordant through time, with spatially rare species remaining rare after extensive extirpations relative to species that were historically more widespread. In contrast, extirpations greatly disrupted patterns of species co-occurrence on both local and regional scales. Over 50% of the species pairs that historically co-occurred (in the same 5  km reach) no longer co-occur anywhere in the Lower Basin, and species pairs that infrequently co-occurred in historic times suffered greater proportional losses than did more widely co-occurring pairs. Such changes in the relationship between spatial rarity and species richness deserve attention because they inhibit conservation planning (decreasing the efficiency of reserve design) and reduce interaction diversity altering opportunities for long-term co-evolutionary change.     

Management implications of the Macquarie Island trophic cascade revisited: a reply to Dowding et al. (2009)

1. The management of non-indigenous species is not without its complications. In Bergstrom et al. 's (2009) study, we demonstrated that feral cats Felis catus on sub-Antarctic Macquarie Island were exerting top-down control on the feral rabbit Oryctolagus cuniculus population, and that the eradication of the cats led to a substantial increase in rabbit numbers and an associated trophic cascade.
2. Dowding et al. (2009) claim our modelling was flawed for various reasons, but primarily that a reduction in the application of the rabbit control agent, Myxoma virus, coinciding with cat removal, was a major driver of rabbit population release.
3. We explore this proposition (as well as others) by examining rates of Myxoma viral release between 1991 and 2006 (with an attenuation factor for the years, 2003–2006) in association with presence/absence of cats against two estimates of rabbit population size. Myxoma viral release was a significant factor in the lower estimates of rabbit population, but the effect was small, and was not significant for higher rabbit population estimates. By contrast, the presence or absence of cats remained highly significant for both estimates.
4. Synthesis and applications. We re-affirm our position that top-down control of rabbit numbers by cats, prior to their eradication, was occurring on Macquarie Island. Nonetheless, we agree with Dowding et al. (2009) that systems with multiple invasive species represent complex situations that require careful scrutiny. Such scrutiny should occur in advance of, during, and following management interventions.     

On the International Code of Area Nomenclature (ICAN): a reply to Zaragüeta-Bagils et al.

In 2007 the Systematic and Evolutionary Biogeographical Association (SEBA) wrote and ratified the first draft of the International Code of Area Nomenclature (ICAN), which was posted subsequently on the SEBA website. The ICAN was published, along with an explanatory discussion, by Ebach et al. ( Journal of Biogeography , 35 , 2008, 1153–1157), an article that is the subject of criticism by Zaragüeta-Bagils et al. ( Journal of Biogeography , 36 , 2009, 1617–1618). We welcome discussion of the issues raised by these authors and respond to them briefly here. For many reasons, we reject the proposition that implementation of the ICAN be postponed until it is flawless. The ICAN has already been implemented. Further, it is the nature of nomenclatural codes to be proposed and then revised periodically to suit our applications. Most importantly, standardization of area names in biogeography is long overdue.     

Within-genotype epigenetic variation enables broad niche width in a flower living yeast

Niche theory is one of the central organizing concepts in ecology. Generally, this theory defines a given species niche as all of the factors that effect the persistence of the species as well as the impact of the species in a given location ( Hutchinson 1957 ; Chase 2011 ). Many studies have argued that phenotypic plasticity enhances niche width because plastic responses allow organisms to express advantageous phenotypes in a broader range of environments ( Bradshaw 1965 ; Van Valen 1965 ; Sultan 2001 ). Further, species that exploit habitats with fine‐grained variation, or that form metapopulations, are expected to develop broad niche widths through phenotypic plasticity ( Sultan & Spencer 2002 ; Baythavong 2011 ). Although a long history of laboratory, greenhouse and reciprocal transplant experiments have provided insight into how plasticity contributes to niche width ( Pigliucci 2001 ), recent advances in molecular approaches allow for a mechanistic understanding of plasticity at the molecular level ( Nicotra et al. 2010 ). In particular, variation in epigenetic effects is a potential source of the within‐genotype variation that underlies the phenotypic plasticity associated with broad niche widths. Epigenetic mechanisms can alter gene expression and function without altering DNA sequence ( Richards 2006 ) and may be stably transmitted across generations ( Jablonka & Raz 2009 ; Verhoeven et al. 2010 ). Also, epigenetic mechanisms may be an important component of an individual’s response to the environment ( Verhoeven et al. 2010 ). While these ideas are intriguing, few studies have made a clear connection between genome‐wide DNA methylation patterns and phenotypic plasticity (e.g. Bossdorf et al. 2010 ). In this issue of Molecular Ecology, Herrera et al. (2012) present a study that demonstrates epigenetic changes in genome‐wide DNA methylation are causally active in a species’ ability to exploit resources from a broad range of environments and are particularly important in harsh environments.     

Speciation genetics of biological invasions with hybridization

The negative effects of human‐induced habitat disturbance and modification on multiple dimensions of biological diversity are well chronicled ( Turner 1996 ; Harding et al. 1998 ; Lawton et al. 1998 ; Sakai et al. 2001 ). Among the more insidious consequences is secondary contact between formerly allopatric taxa ( Anderson & Hubricht 1938 ; Perry et al. 2002 ; Seehausen 2006 ). How the secondary contact will play out is unpredictable ( Ellstrand et al. 2010 ), but if the taxa are not fully reproductively isolated, hybridization is likely, and if the resulting progeny are fertile, the eventual outcome is often devastating from a conservation perspective ( Rhymer & Simberloff 1996 ; Wolf et al. 2001 ; McDonald et al. 2008 ). In this issue of Molecular Ecology, Steeves et al. (2010) present an analysis of hybridization between two avian species, one of which is critically endangered and the other of which is invasive. Their discovery that the endangered species has not yet been hybridized to extinction is promising and not what one would necessarily expect from theory.     

Genetics of personalities: no simple answers for complex traits

Identifying the genes that underlie phenotypic variation in natural populations, and assessing the consequences of polymorphisms at these loci for individual fitness are major objectives in evolutionary biology. Yet, with the exception of a few success stories, little progress has been made, and our understanding of the link between genotype and phenotype is still in its infancy. For example, although body length in humans is largely genetically determined, with heritability estimates greater than 0.8, massive genome‐wide association studies (GWAS) have only been able to account for a very small proportion of this variation ( Gudbjartsson et al. 2008 ). If it is so difficult to explain the genetics behind relatively ‘simple’ traits, can we envision that it will at all be possible to find genes underlying complex behavioural traits in wild non‐model organisms? Some notable examples suggest that this can indeed be a worthwhile endeavour. Recently, the circadian rhythm gene Clock has been associated with timing of breeding in a wild blue tit population ( Johnsen et al. 2007 ; Liedvogel et al. 2009 ) and the Pgi gene to variation in dispersal and flight endurance in Glanville fritillary butterflies ( Niitepold et al. 2009 ). A promising candidate gene for influencing complex animal personality traits, also known as behavioural syndromes ( Sih et al. 2004 ), is the dopamine receptor D4 (DRD4) gene. Within the last decade, polymorphisms in this gene have been associated with variation in novelty seeking and exploration behaviour in a range of species, from humans to great tits ( Schinka et al. 2002 ; Fidler et al. 2007 ). In this issue, Korsten et al. (2010) attempt to replicate this previously observed association in wild‐living birds, and test for the generality of the association between DRD4 and personality across a number of European great tit populations.     

The importance of rare species: a trait‐based assessment of rare species contributions to functional diversity and possible ecosystem function in tall‐grass prairies

The majority of species in ecosystems are rare, but the ecosystem consequences of losing rare species are poorly known. To understand how rare species may influence ecosystem functioning, this study quantifies the contribution of species based on their relative level of rarity to community functional diversity using a trait‐based approach. Given that rarity can be defined in several different ways, we use four different definitions of rarity: abundance (mean and maximum), geographic range, and habitat specificity. We find that rarer species contribute to functional diversity when rarity is defined by maximum abundance, geographic range, and habitat specificity. However, rarer species are functionally redundant when rarity is defined by mean abundance. Furthermore, when using abundance‐weighted analyses, we find that rare species typically contribute significantly less to functional diversity than common species due to their low abundances. These results suggest that rare species have the potential to play an important role in ecosystem functioning, either by offering novel contributions to functional diversity or via functional redundancy depending on how rare species are defined. Yet, these contributions are likely to be greatest if the abundance of rare species increases due to environmental change. We argue that given the paucity of data on rare species, understanding the contribution of rare species to community functional diversity is an important first step to understanding the potential role of rare species in ecosystem functioning.     

Geographic patterns in the distribution of Palearctic songbirds

A database was created of digitized equal area distribution maps of 3,036 phylogenetic species of Palearctic songbirds. Biogeographic patterns are reported for two data sets: (1) including all passeriform bird species reported as breeding within the boundaries of our study map, (2) passeriform species restricted in their distribution to our study region, thus excluding the partly extra-limital taxa. With respect to the data set excluding partly extra-limital taxa, the average range size is 238 grid cells (grid cell area: 4,062 km²). Analysis of the geographic distribution of species richness for the full data set showed several hotspot regions, mostly located in mountainous areas. The index of range-size rarity identified similar hotspot regions as that for species richness, albeit that the range-size rarity de-emphasized the central Siberian hotspot. Range-size rarity hotspots that are not evident on the measure of species richness concern a great number of islands. Much more prominent on the index of range-size rarity are the Atlas Mountains of northern Africa, the Jabal al Akhdar region in NE Libya, and the eastern border of the Mediterranean. Restricting the analysis of geographic variation to the 25% of the species with smallest ranges resulted in a greatly simplified pattern of hotspots. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Forms of rarity of tree species in the southern Brazilian Atlantic rainforest

The assessment of species rarity considers local abundance (scarce or abundant population), habitat affinity (stenoecious or euryecious species), and geographic distribution (stenotopic or eurytopic species). When analyzed together these variables classify species into eight categories, from common species to those having small populations, unique habitats, and restricted geographic distribution (form 7), as proposed by Rabinowitz in 1981. Based on these categories, it is possible to calculate the frequency of the different forms of rarity of the species present in a given site. The Brazilian Atlantic rainforest is considered a hotspot of the world biodiversity harboring many endemic species, which have restricted geographic distribution. Our objective was to identify the forms of rarity of tree species and their proportions in the southern portion of the Brazilian Atlantic rainforest using Rabinowitz’s forms of rarity. All the seven forms of rarity are present in the 846 tree species we analyzed: 46% eurytopic and 54% stenotopic, 73% euryecious and 27% stenoecious, 76% locally abundant and 24% locally scarce species. Eurytopic, euryecious locally abundant species accounted for 41.1%, whereas 58.9% were somehow rare: 4.5% eurytopic, euryecious locally scarce, 0.2% eurytopic, stenoecious locally abundant, 0.1% eurytopic, stenoecious locally scarce, 19.5% stenotopic, euryecious locally abundant, 8.0% stenotopic, euryecious locally scarce, 15.6% stenotopic, stenoecious locally abundant, and 11.0% stenotopic, stenoecious locally scarce. Considering that the most restrictive forms of rarity precedes extinction, the application of Rabinowitz’s system demonstrated that most tree species of the southern Brazilian Atlantic rainforest are threatened due to their restricted geographic distribution, restriction to a single habitat, reduced local abundance, or even to a combination of these variables.     

Rarity and species/area relationships of vascular plants in deciduous woods, western Norway - applications to nature reserve selection

The Rabinowitz s model of rarity was applied to a vascular plant census list from 60 deciduous woods in western Norway By applying information from distribution maps and plant sociological literature from western Norway it was possible to obtain data on geographical distribution, habitat specificity, and maximum local population size at the regional-scale of western Norway This enabled a comparison between rarity at the local scale and rarity at the regional scale At the local scale rarity was primarily due to narrow geographic distribution At the regional scale, however, the most frequent form of rarity was due to restricted habitat specificity The species/area relationship and the SLOSS effect for the rare species at the regional scale are compared with patterns involving the total species list It is shown that a single large wood supports fewer regional-scale rare species than do combinations of two small woods of equal area The species/area relationship for species with small population sizes at the regional scale has a different slope from the species/area relationship for all species Area is a better predictor of regional-scale rarity than is the number of common species     

Calcareous sponges of the genera Clathrina and Guancha (Calcinea, Calcarea, Porifera) of Norway (north-east Atlantic) with the description of five new species

The taxonomy and distribution of 11 species of calcareous sponges of the subclass Calcinea from the Norwegian coast are reviewed. The Norwegian Calcinea represents a mixture of southern boreal/boreal and boreoarctic species, and the calcinean sponge fauna of northern Norway has strong similarities to the Greenlandic and the White Sea/Barents Sea sponge faunas. Most Norwegian Calcinea have their main distribution between 20 and 100 m depth, although some species are found only in the shallow sublittoral or from sublittoral to abyssal depths. Six species were previously reported in the area: Clathrina coriacea (Montagu, 1818), Clathrina cribrata Rapp et al ., 2001, Clathrina nanseni (Breitfuss, 1896), Clathrina septentrionalis Rapp et al ., 2001, Guancha blanca Miklucho-Maclay, 1868 and Guancha lacunosa (Johnston, 1842). Five species are new to science: Clathrina corallicola , Clathrina jorunnae , Guancha arnesenae , Guancha camura , and Guancha pellucida spp. nov. A key to the known Norwegian Calcinea is provided.  © 2006 The Linnean Society of London, Zoological Journal of the Linnean Society , 2006, 147 , 331–365.     

Is there evidence that the Chinese paddlefish (Psephurus gladius) still survives in the upper Yangtze River? Concerns inferred from hydroacoustic and capture surveys, 2006–2008

Due to the rarity of Chinese paddlefish ( Psephurus gladius ), very little information is available on this species. In order to save this critically endangered giant species, four large-range hydroacoustic surveys (using an echo sounder with a 199 kHz, 6.8° split-beam transducer) and capture surveys (by drift nets and setlines) were conducted in the upper Yangtze River during 2006–2008. According to the target strength (TS) study on Polyodon spathula ( Hale et al., 2003 ) and Love's formula about TS-fish length relationships ( Love, 1971 ), the four acoustic surveys identified nine potential targets (TS > −26.29 dB) of P. gladius , two (TS > −22.40 dB) of them very probably the fish species sought. A total of 4762 setlines, 111 anchored setlines and 950 drift net catches were conducted in which 472 large fish specimens of various species were caught. However, no single P. gladius was caught directly. The gear used did not allow quantitative capture over rough ground with deep holes, perhaps allowing some large fish to effectively hide or escape; the hydroacoustic signals indicated this as likely. In any case, it is strongly suggested that P. gladius is on the verge of extinction and further rigid measures are proposed to save the very few remaining specimens.     

Patterns of rare fish and aquatic insects in a southwestern French river catchment in relation to simple physical variables

Most of our current understanding of rarity has come from studies of terrestrial plants and animals, whereas freshwater habitats remain poorly documented under this topic. Here we considered the spatial distribution patterns of rarity at the river catchment scale, for five freshwater taxa (fish, Ephemeroptera, Plecoptera, Trichoptera and Coleoptera) in southwestern France. The data were collected at 554 and 155 sampling sites for fish and aquatic insects, respectively. General Linear Modelling was used to assess the influence of some typological variables (elevation, stream order, distance from source, and reach slope) on local numbers of rare species (restricted range). The relative numbers of rare species per taxa varied from 16% (Plecoptera) to 59% (Trichoptera). GLM chiefly yielded highly significant correlations between rarity and distance from the source and/or elevation for all taxa, showing that numbers of rare stream species increase towards downstream areas within the stream system. The spatial patterns in rarity for the different study taxa were rather concordant, probably as a result of similar responses to environmental conditions. By focusing on integrative variables, we emphasized the influence of river typology on the rarity of aquatic animals. Areas which carry rare species may concentrate an important fraction of the regional biodiversity. If end-users need geographic models (i.e. maps) to design river management frameworks, numerical patterning is needed to provide theoretical backgrounds: by predicting what the rarity should be like in a given area, we can provide explicit spatial schemes that may be useful to target further research, and to implement management options.     

Hybrid speciation in birds: allopatry more important than ecology?

Hybrid speciation was once thought to be rare in animals, but over the past decade, improved molecular analysis techniques and increased research attention have allowed scientists to uncover many examples. In this issue, two papers ( Elgvin et al. 2011 ; Hermansen et al. 2011 ) present compelling evidence for the hybrid origin of the Italian sparrow based on nuclear and mitochondrial DNA sequences, microsatellites, and plumage coloration. These studies point to an important role for geographic isolation in the process of hybrid speciation, and provide a starting point for closer examination of the genetic and behavioural mechanisms involved.     

How did an annual plant react to Pleistocene glaciations? Postglacial history of Rhinanthus angustifolius in Europe

The impact of climate fluctuations during the Pleistocene on the geographic structure of genetic variation in plant populations is well documented, but there is a lack of studies of annual species at the European scale. The present study aimed to infer the history of the widespread European annual Rhinanthus angustifolius C. C. Gmelin (Orobanchaceae). We explored variation in chloroplast DNA (cpDNA) sequences and amplified fragment length polymorphism (AFLP) in twenty-nine populations covering the entire distribution area of the species. Five AFLP groups were identified, suggesting at least two glacial refugial areas: one area in southwestern Europe and one large eastern area in the Balkan/Caucasus. Recolonization of previously glaciated areas mainly took place from the east of Europe. Despite the difference in life-history traits, the patterns found for the annual R. angustifolius show similarities with those of perennial species in terms of genetic diversity and geographic organization of genetic variation. Although organelle markers have typically been preferred in phylogeographic studies, the cpDNA variation in R. angustifolius did not show any clear geographic structure. The absence of geographic structure in the cpDNA variation may reflect persistence of ancestral polymorphisms or hybridization and introgression with closely-related species.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 98 , 1–13.     

Island size is not the only consideration. Ranking priorities for the conservation of butterflies on Italian offshore islands

Ecological and historical factors virtually create a unique faunal assemblage on each island. From this perspective every island deserves protection. However, economic limitations usually restrict conservation efforts to particularly important areas. As part of the SLOSS issue (the relative importance of single large or several small areas), there is the long debated question of whether it is better to protect few large areas (islands) or several small areas (islands). Here, we assess the butterfly faunas of the Italian offshore islands, using several biodiversity measures, in order to highlight priorities for conserving butterfly richness, rarity and endemicity. First, the nested pattern of butterfly fauna was investigated to determine the relative importance of large and small islands. Then, residuals were assessed for the species-area relationship and for multiple regressions of richness, rarity and endemicity against geographic variables. Subsequently, two other indices were calculated: Biodiversity Conservation Concern and an index scoring islands in the order that maximizes the cumulative percentage of total, endemic, and rare species. The results clearly indicate that although greatest concern is for the island having the largest butterfly fauna in the sample (Elba), the importance of several small islands should not be ignored. This is primarily due to the substantial impact of source areas and consequently the occurrence of several rare and endemic species occurring on small islands as well as on large islands.