Comparison of ciliate communities in the anoxic hypolimnia of three lakes: general features and the influence of lake characteristics

The ciliate communities and their food sources were investigatedin the anoxic hypolimnia of three lakes with differing waterchemistry. Bacterial biomass and, as a result, the biomass ofbactenvorous ciliates were correlated with lake trophy. Additionally,high sulfate and sulfide concentrations led to high bacterialbiomass of sulfate reducers and anaerobic phototrophic and heterotrophicbacteria, which in turn sustained large ciliate populations.The anaerobic ciliate communities of the lakes shared many characteristics.They were comprised of the same or closely related species;this was attributed to a low diversity of food sources. Ciliateto prey biomass ratios were 1.2–3.8% which is consistentwith a low theoretical growth efficiency of anaerobic metabolism.Grazing pressure on anaerobic ciliates by metazoa was insignificant.In all three lakes, ciliate populations showed distinct verticalnon-random distribution patterns which were often correlatedwith the distribution of the corresponding food sources. Itis suggested that the microbial communities in anoxic waterbodies are largely influenced by few common environmental conditionsand are therefore often inhabited by similarly structured ciliatecommunities.     

Studies on ciliated protozoa in eutrophic lakes: 2. Field and laboratory studies on the effects of oxygen and other chemical gradients on ciliate distribution

An investigation into the spatial distribution of hypolimnetic ciliates in three small eutrophic lakes during the period of summer stratification was carried out. Peak ciliate densities were found to occur at the oxic/anoxic boundary, ciliate numbers declining with increasing depth within the hypolimnion. The ciliates only occurred in aerobic water where oxygen levels were less than about 0.5 mgl^–1 Laboratory experiments demonstrated that the ciliates swim upwards under anaerobic conditions but swim rapidly downwards under aerobic conditions. Further laboratory experiments showed that although the bulk of the population occured within anaerobic water, the hypolimnetic ciliates are aerobes and cannot survive indefinite anoxia. Despite the demonstrable toxicity of high levels of ammonia and sulphide, it was probably excesive distance from an available source of oxygen that excluded the ciliates from the lowest levels of the hypolimnion. Possible mechanisms which allowed these aerobic ciliates to colonise anaerobic water are considered.     

Diversity and Distributional Patterns of Ciliates in Guaymas Basin Hydrothermal Vent Sediments

Little is known about protists at deep‐sea hydrothermal vents. The vent sites at Guaymas Basin in the Gulf of California are characterized by dense mats of filamentous pigmented or nonpigmented Beggiatoa that serve as markers of subsurface thermochemical gradients. We constructed 18S rRNA libraries to investigate ciliate assemblages in Beggiatoa mats and from bare sediments at the Guaymas vent site. Results indicated a high diversity of ciliates, with 156 operational taxonomic units identified in 548 sequences. Comparison between mat environments demonstrated that ciliate and bacterial assemblages from pigmented mats, nonpigmented mats, and bare sediments were significantly different and highly correlated with bacterial assemblages. Neither bacterial nor ciliate assemblages were correlated with environmental factors. The most abundant ciliates at Guaymas were more likely to be represented in clone libraries from other hydrothermal, deep‐sea, and/or anoxic or microaerophilic environments, supporting the hypothesis that these ciliate species are broadly distributed. The orange mat environment included a higher proportion of ciliate sequences that were more similar to those from other environmental studies than to cultured ciliate species, whereas clone libraries from bare sediments included sequences that were the most highly divergent from all other sequences and may represent species that are endemic to Guaymas.     

Seasonal development of hypolimnetic ciliate communities in a eutrophic pond

Abstract The ciliated protozoan communities in the hypolimnion of a highly produtive pond were investigated over two years. Three physiological groups could be distinguished: stratified water column; (b) anaerobic ciliates with endosymbiotic methanogens; and (c) anaerobes without endosymbiotic methanogens. Both groups of anaerobes were confined to the anoxic zone of the hypolimnion. Community biomass was dominated by microaerobic ciliates which had on average 20 times larger cells than anaerobic ciliates. Abundance and biomass of microaerobic ciliates decreased over the summer, while anaerobic ciliates increased. This reflected a spatial shift in the availability of inorganic nutrients and, as a result, of ciliate food from the epi- and metalimnion to the hypolimnion. The low biomass production of anaerobic ciliates was consistent with the low theoretical growth efficiency of anaerobic metabolism. Ciliate species displayed characteristic spatial and seasonal distribution patterns within the water column which were similar in both years investigated. Spatial and temporal distribution was mainly governed by two factors: (1) the distribution of dissolved oxygen; and (2) the availability of food. Distribution patterns were not related to chemical gradients other than the oxygen gradient, but they were correlated with the distribution of major food sources.     

Diversity and geographic distribution of ciliates (Protista: Ciliophora)

About 4,500 free-living ciliate morphospecies have been described, applying an average synonymy rate of 20%. We estimate that 83–89% of the ciliate diversity is still undescribed, using the following probabilities: detailed habitat studies suggest that the described number of morphospecies must be doubled: 4,500 → 9,000; this figure has to be increased by about 50% due to species with similar interphase morphology but different resting cysts: 9,000 → 13,500; the genetic and molecular data suggest that this value must be doubled or trebled: 13,500 → 27,000 to 40,000 free-living, biological ciliate species. The knowledge on geographic distribution of ciliates heavily depends on flagship species and statistical analyses because reliable faunistic studies are rare and molecular data are still in its infancy. We present a list of 52 ciliate flagship species as a testable hypothesis, i.e., the hypothesis of restricted distribution of certain ciliate species must be refused when a considerable number of them is found in all or most biogeographic regions. Flagship species and statistical analyses consistently show Gondwanan and Laurasian ciliate communities, suggesting that the split of Pangaea deeply influenced ciliate distribution and rare species play a key role in geographic differentiation. However, there is also substantial evidence for continental, regional, and local endemism of free-living ciliates. The molecular studies usually show a high level of genetic diversity underlying ciliate morphospecies, suggesting that morphologic and molecular evolution may be decoupled in many ciliate species. Molecular studies on ciliate biogeography are at variance, possibly because most are still focusing on single molecular markers. In sum, the data indicate that ciliate biogeography is similar to that of plants and animals, but with an increased proportion of cosmopolites, favouring the moderate endemicity model. Special Issue: Protist diversity and geographic distribution. Guest editor: W. Foissner.     

Prevalent Ciliate Symbiosis on Copepods: High Genetic Diversity and Wide Distribution Detected Using Small Subunit Ribosomal RNA Gene

Toward understanding the genetic diversity and distribution of copepod-associated symbiotic ciliates and the evolutionary relationships with their hosts in the marine environment, we developed a small subunit ribosomal RNA gene (18S rDNA)-based molecular method and investigated the genetic diversity and genotype distribution of the symbiotic ciliates on copepods. Of the 10 copepod species representing six families collected from six locations of Pacific and Atlantic Oceans, 9 were found to harbor ciliate symbionts. Phylogenetic analysis of the 391 ciliate 18S rDNA sequences obtained revealed seven groups (ribogroups), six (containing 99% of all the sequences) belonging to subclass Apostomatida, the other clustered with peritrich ciliate Vorticella gracilis. Among the Apostomatida groups, Group III were essentially identical to Vampyrophrya pelagica, and the other five groups represented the undocumented ciliates that were close to Vampyrophrya/Gymnodinioides/Hyalophysa. Group VI ciliates were found in all copepod species but one (Calanus sinicus), and were most abundant among all ciliate sequences obtained, indicating that they are the dominant symbiotic ciliates universally associated with copepods. In contrast, some ciliate sequences were found only in some of the copepods examined, suggesting the host selectivity and geographic differentiation of ciliates, which requires further verification by more extensive sampling. Our results reveal the wide occurrence and high genetic diversity of symbiotic ciliates on marine copepods and highlight the need to systematically investigate the host- and geography-based genetic differentiation and ecological roles of these ciliates globally.     

Genetic analysis of ciliates living on the groundwater amphipod Crangonyx islandicus (Amphipoda: Crangonyctidae)

Two endemic subterranean freshwater amphipod species have been discovered in groundwater of the volcanic active zone in Iceland, Crangonyx islandicus and Crymostygius thingvallensis. At least five different ciliate sequences were isolated from C. islandicus and the analysis of variation at the 18S ribosomal DNA gene suggests that they present previously unsequenced species, from the orders Apostomatida and Philasterida. Apostome ciliates are well known to be exuviotrophic epibionts on crustaceans. Analyses of ciliate epibionts from different groundwater amphipod species from North America and mainland Europe revealed distinct groups of ciliates and higher diversity on the epigean amphipod Crangonyx pseudogracilis. Analysis of geographic patterns of the most common ciliate within Iceland revealed population differentiation supporting limited current connectivity between the different groundwater systems. Our study reports an occurrence of previously undescribed ciliate species in a groundwater ecosystem characterized by low species diversity.     

Role of anaerobic ciliates in planktonic food webs: abundance, feeding, and impact on bacteria in the field

We studied the dynamics of two populations of anaerobic ciliates, Plagiopyla sp. and Metopus sp., and of their potential prey, heterotrophic and phototrophic purple bacteria, in Lake Cisó throughout a 1-year cycle. The abundance of both ciliates was very low (less than 2 individuals per ml). During mixing, Plagiopyla ciliates exhibited high clearance rates (about 100 nl ciliate h), its integrated abundance increased with a net doubling time of 47 days, and its potential doubling times, as calculated from the number of bacteria consumed, ranged between 5 and 8 days. During stratification, the activity of Plagiopyla ciliates was reduced and the population decreased; this was related to the higher amounts of sulfide present. The impact of predation by the Plagiopyla population on bacterioplankton was found to be insignificant, less than 0.1% of bacterial biomass consumed per day. Thus, anaerobic ciliates cannot control the bacterioplankton in Lake Cisó because of both the low abundance over the period studied and the low feeding rates during certain periods. A review of available field studies suggests that this conclusion can be extrapolated to most other anoxic systems.     

The symbiotic intestinal ciliates and the evolution of their hosts

The evolution of sophisticated differentiations of the gastro-intestinal tract enabled herbivorous mammals to digest dietary cellulose and hemicellulose with the aid of a complex anaerobic microbiota. Distinctive symbiotic ciliates, which are unique to this habitat, are the largest representatives of this microbial community. Analyses of a total of 484 different 18S rRNA genes show that extremely complex, but related ciliate communities can occur in the rumen of cattle, sheep, goats and red deer (301 sequences). The communities in the hindgut of equids (Equus caballus, Equus quagga), and elephants (Elephas maximus, Loxodonta africanus; 162 sequences), which are clearly distinct from the ruminant ciliate biota, exhibit a much higher diversity than anticipated on the basis of their morphology. All these ciliates from the gastro-intestinal tract constitute a monophyletic group, which consists of two major taxa, i.e. Vestibuliferida and Entodiniomorphida. The ciliates from the evolutionarily older hindgut fermenters exhibit a clustering that is specific for higher taxa of their hosts, as extant species of horse and zebra on the one hand, and Africa and Indian elephant on the other hand, share related ciliates. The evolutionary younger ruminants altogether share the various entodiniomorphs and the vestibuliferids from ruminants.     

Protist diversity in suboxic and sulfidic waters of the Black Sea

The oxic-anoxic transition zone of the Black Sea comprises a large suboxic zone as well as anoxic and sulfidic waters. While the prokaryotes and biogeochemical cycles that characterize this zone have been frequently studied, little is known about the diversity or ecology of its microbial eukaryotes. Here, we present the first broad qualitative report of the protist species composition in the Black Sea redoxcline using molecular tools. Fingerprint analysis from the whole redoxcline revealed a complex community structure of metabolically active protists with distinct shifts along the redox gradient. Additionally, 18S rRNA gene clone libraries were used to compare protist species composition of suboxic and sulfidic water layers. Among the ciliates, sequences related to Pleuronema and Strombidium were dominant in both water layers whereas sequences affiliated with anaerobic plagiopylids and Cyclidium were detected only in the sulfidic zone. Among the flagellates, mainly stramenopiles (mostly bicosoecids and chrysophytes) occurred throughout the redoxcline. In the sulfidic zone we found stramenopile sequences but also euglenozoans, jakobids and choanoflagellates that were related to clonal sequences from other anoxic marine habitats, thus indicating the existence of globally distributed groups of anoxic flagellates. Higher species diversity in the sulfidic zone and about twice as many novel sequence types of ciliates and stramenopiles compared with the suboxic layer emphasizes the importance of anoxic, sulfidic waters as habitat for high protist diversity although the function of these organisms is yet unknown.     

Analysis of the community structure of planktonic ciliated protozoa relative to trophic state in Florida lakes

The planktonic ciliate populations of 30 Florida lakes constituting a broad trophic gradient were examined to determine the response of protozoan community structure to increasing eutrophication. Both ciliate abundance and biomass were strongly related to lake trophic state. Comparison of the Florida data base with a comparable north temperate lake group indicated that subtropical lakes generally possess higher ciliate abundance and biomass at a given trophic state than temperate lakes. However the equations derived for each data base were not significantly different. Community diversity and species richness increased with increasing lake productivity. Highly acidic lakes displayed significantly reduced diversity and numbers of species when contrasted with nonacidic oligotrophic lakes. Small-bodied (< 30 um) ciliates dominated all lakes but were proportionally less important in oligotrophic lakes. Presence-absence data produced three assemblages: an ubiquitous association of primarily small ciliate taxa, a group of large ciliates mainly restricted to eutrophic-hypereutrophic lakes, and a very large ciliate,Stentor niger, which dominated the protozoan communities of acidic oligotrophic lakes.     

甘肃天水麦积山风景名胜区土壤纤毛虫的物种多样性

用活体观察和固定染色方法对麦积山风景名胜区土壤纤毛虫物种多样性进行了研究。共鉴定到隶属于3纲12目41科55属的土壤纤毛虫115种,其中包括11个未定名种和26个中国土壤纤毛虫新纪录种。街子温泉景区、曲溪景区、麦积山石窟区、石门山和仙人崖景区各分布有47、46、44、33和26种,大弹跳虫、似织毛虫、膨大肾形虫、僧帽肾形虫、迅捷肾形虫、吻四膜虫、长刀口虫和苔藓刀口虫为广布物种。前口目和下毛目为风景名胜区土壤纤毛虫群落中的优势类群,肾形目和盾纤目为次优势类群,侧口目、吸管目和寡毛目为罕见类群。风景名胜区土壤纤毛虫物种多样性与我国已有研究报道的其他地区的均极不相似。研究结果表明,风景名胜区土壤纤毛虫物种十分丰富,特有和稀有物种繁多,群落结构复杂而特殊;土壤和水生纤毛虫群落物种组成极不相似,土壤和水生纤毛虫群落是不同的2个独立群落。     

Evolution of Histone H4 and H3 Genes in Different Ciliate Lineages

The histones H4 are known as highly conserved proteins. However, in ciliates a high degree of variation was found compared both to other eukaryotes and between the ciliate species. To date, only H4 histones of species belonging to two distantly related classes have been investigated. In order to obtain more detailed information on histone H4 variation in ciliates we undertook a comprehensive sequence analysis of PCR-amplified internal H4 fragments from 12 species belonging to seven out of the nine currently recognized ciliate classes. In addition, we used PCR primers to amplify longer fragments of H3 and H4 genes including the intergenic region. The encoded amino acid sequences reveal a high number of differences when compared with those of other eukaryotes and the ciliate species investigated. Furthermore, in some species H4 gene variants were detected, which result in amino acid differences. The greatest number of substitutions and insertions found was in the amino terminal region of the H4 histones. However, all sequences possess a conserved region corresponding to those of all other eukaryotic H4 histones. The histone gene variations were used to reconstruct phylogenetic relationships. The tree from our data matches perfectly with the ribosomal RNA data: The heterotrichs, which were considered as a late branching lineage, diverge at the base of the ciliate tree and groups formerly thought to represent ancestral lineages now appear as highly derived ciliates. Received: 4 April 1997 / Accepted: 1 August 1997     

Ciliates along Oxyclines of Permanently Stratified Marine Water Columns

Studies of microbial communities in areas of the world where permanent marine water column oxyclines exist suggest they are “hotspots” of microbial activity, and that these water features and the anoxic waters below them are inhabited by diverse protist taxa, including ciliates. These communities have minimal taxonomic overlap with those in overlying oxic water columns. Some ciliate taxa have been detected in multiple locations where these stable water column oxyclines exist; however, differences in such factors as hydrochemistry in the habitats that have been studied suggest local selection for distinct communities. We compare published data on ciliate communities from studies of deep marine water column oxyclines in Caricao Basin, Venezuela, and the Black Sea, with data from coastal, shallower oxycline waters in Framvaren and Mariager fjords, and from several deep‐sea hypersaline anoxic basins in the Eastern Mediterranean Sea. Putative symbioses between Bacteria, Archaea, and ciliates observed along these oxyclines suggests a strategy of cooperative metabolism for survival that includes chemosynthetic autotrophy and exchanges of metabolic intermediates or end products between hosts and their prokaryotic partners.     

土壤纤毛虫群落对退耕还林生态恢复的响应——以侧柏林为例

为了了解土壤纤毛虫群落对退耕还林区生态恢复下土壤环境变化的响应及尝试利用土壤纤毛虫群落特征评价退耕还林生态恢复的效果,于2010年3月至9月采用"非淹没培养皿法"、活体观察法、蛋白银染色法和Foissner计数法对甘肃陇南武都退耕还林区5个不同恢复阶段的样点和1个荒草坡对照样点的土壤纤毛虫群落特征进行了研究,同时测定了p H值、温度、含水量及速效磷、有效钾、铵态氮、有机质和有机碳含量等土壤环境因子并分析了生态恢复条件下土壤纤毛虫群落特征与土壤环境因子的相关性。研究中共鉴定到71种纤毛虫,隶属于3纲、10目、22科、29属。研究发现,不同恢复年限的土样中土壤纤毛虫的物种分布存在明显差异,并随恢复时间的延长,样点间物种相似性减小,群落组成复杂化,物种数、种群密度和物种多样性指数总体均呈增长趋势。优势类群也发生了演替,由恢复初期的肾形目演替到后期的下毛目。相关性分析结果表明,在生态恢复条件下,土壤有机质和铵态氮含量是影响土壤纤毛虫群落结构稳定性的主要因素,不同纤毛虫类群对生态恢复的响应存在差异。冗余分析显示,土壤纤毛虫群落很好地响应了生态恢复过程中土壤环境条件的变化。     

Use of Tetrahymena thermophila to study the role of protozoa in inactivation of viruses in water

The ability of a ciliate to inactivate bacteriophage was studied because these viruses are known to influence the size and diversity of bacterial populations, which affect nutrient cycling in natural waters and effluent quality in sewage treatment, and because ciliates are ubiquitous in aquatic environments, including sewage treatment plants. Tetrahymena thermophila was used as a representative ciliate; T4 was used as a model bacteriophage. The T4 titer was monitored on Escherichia coli B in a double-agar overlay assay. T4 and the ciliate were incubated together under different conditions and for various times, after which the mixture was centrifuged through a step gradient, producing a top layer free of ciliates. The T4 titer in this layer decreased as coincubation time increased, but no decrease was seen if phage were incubated with formalin-fixed Tetrahymena. The T4 titer associated with the pellet of living ciliates was very low, suggesting that removal of the phage by Tetrahymena inactivated T4. When Tetrahymena cells were incubated with SYBR gold-labeled phage, fluorescence was localized in structures that had the shape and position of food vacuoles. Incubation of the phage and ciliate with cytochalasin B or at 4 degrees C impaired T4 inactivation. These results suggest the active removal of T4 bacteriophage from fluid by macropinocytosis, followed by digestion in food vacuoles. Such ciliate virophagy may be a mechanism occurring in natural waters and sewage treatment, and the methods described here could be used to study the factors influencing inactivation and possibly water quality.     

A statistical approach to estimate soil ciliate diversity and distribution based on data from five continents

A total of 359 soil samples collected from five continents (Africa, Asia, Australia, Europe and South America) were investigated for the presence/absence of soil ciliate species. Merging records by species identity, we have compiled a master data list (species by sample matrix). In the list, a total of 964 soil ciliate species (644 described and 320 undescribed) are recorded. The species distributions within the 359 samples and across the five continents are examined. The frequency distribution of the species over samples is used for global diversity estimation. A statistical ACE (abundance‐based coverage estimation) model which links observed data to unseen species is applied to assess regional and global soil ciliate species richness. The model, whose reliability was tested by its power to predict the number of new species in additional samples from Africa, may resolve the controversial issue on global species diversity of soil ciliates. Although an accurate point estimate is not feasible due to severe undersampling, the statistical model enables us to obtain a minimum regional diversity and global species diversity. A consistent finding over all five continents is that at least half of the species diversity is still undiscovered. Our model also yields a global soil ciliate diversity of at least 1900 species, that is, doubles the number of currently known species, and thus diversity is relatively high. This is consistent with the finding of Foissner, who used a probability‐based method. Soil ciliate distributions between continent pairs are analyzed by adjusted abundance‐based similarity/overlap indices. These new indices account for the effect of unseen species and also reduce the bias generated by undersampling. The adjusted abundance‐based Jaccard (or Sørensen) index shows that there is about 30% (18% for Sørensen) dis‐similarity between any two continents, supporting the moderate endemicity model. The results are discussed with respect to protist species distribution, that is, whether they are cosmopolitan or of restricted distribution.     

Comparative analysis of the mitochondrial cytochrome c oxidase subunit I (COI) gene in ciliates (Alveolata,Ciliophora) and evaluation of its suitability as a biodiversity marker

The mitochondrial cytochrome c oxidase subunit 1 (COI) gene of ciliates was first successfully sequenced in species of the genera Tetrahymena and Paramecium (Class Oligohymenophorea). The sequence of the COI gene is extremely divergent from other eukaryotes and includes an insert, which is over 300 nucleotides long. In this study, we designed a primer pair that successfully amplified the COI gene of ciliates from five different classes: Heterotrichea, Spirotrichea, Oligohymenophorea, Nassophorea and Colpodea. These classes represent the diversity of the phylum Ciliophora very well, since they are widely distributed on the ciliate small subunit rRNA tree. The amplified region is approximately 850 nucleotides long and corresponds to the general barcoding region; it also includes the insert region. In this study, 58 new COI sequences from over 38 species in 13 orders are analysed and compared, and distance trees are constructed. While the COI gene shows high divergence within ciliates, the insert region, which is present in all classes, is even more divergent. Genetic distances calculated with and without the insert region remain in the same range at the intraspecific level, but they differ considerably at or above genus level. This suggests that the entire barcoding region is under similar selective constraints and that the evolutionary rate of the ciliate COI is extremely high and shows unequal rate variation. Although many problems still remain regarding standardization of barcoding methods in ciliates, the development of a universal or almost universal primer combination for the Phylum Ciliophora represents important progress. As shown in four examples, the resolution of COI at the intraspecific level is much greater than that of any nuclear genes and shows great potential to (1) identify species based on molecular data if a reliable database exists, and (2) resolve the relationships of closely related ciliate taxa and uncover cryptic species.     

Monoxenic culture of the anaerobic ciliate Trimyema compressum Lackey

Sapropelic ciliates from anoxic mud samples were enriched and cultivated in monoculture together with natural food bacteria growing on cellulose. The ciliates lacked cytochrome oxidase and contained bluish fluorescent endosymbionts. One of the anaerobic ciliates, Trimyema compressum, contained methanogenic bacteria as was shown by methane formation. During continued cultivation, T. compressum gradually lost its endosymbionts. With SEM microscopy no episymbiotic bacteria could be detected.From enrichment cultures of T. compressum, anaerobic bacteria were isolated in pure culture. One of the strains, a Bacteroides spec., proved capable of serving as food bacteria, thus allowing establishment of monoxenic T. compressum cultures. These cultures exhibited a requirement for sterols as growth factors. The doubling time of this ciliate was 13 h at 28°C. The highest yield obtained was 2100 cells/ml.Dedicated to Holger W. Jannasch on the occasion of his 60th birthday     

Chemosensory Behaviour of Strombidium purpureum, an Anaerobic Oligotrich with Endosymbiotic Purple Non-Sulphur Bacteria

ABSTRACT. Strombidium purpureum Kahl, is an anaerobic oligotrichous ciliate with endosymbiotic phototrophic bacteria. Like other anaerobic ciliates, S. purpureum reacts to O₂-pressure. In the light, the ciliates avoid even traces of O₂ (< 1% atmospheric saturation). In the dark, however, the ciliates accumulate in water with a pO₂ of 1–4% atmospheric saturation. Experiments show that ciliates which have accumulated in the dark under microaerophilic conditions react when the light is turned on, and their ability to escape is enhanced by steep O₂-gradients. The ciliates orient themselves in O₂-gradients by a series of phobic responses. They tumble whenever they swim towards a higher O₂-tension and thus they eventually all swim in the direction of lower pO₂. The ecological implications of such behaviour are discussed.