Recognition of Host Plant Volatiles by Pheidole minutula Mayr (Myrmicinae), an Amazonian Ant-Plant Specialist

In the tropics, several ant species are obligate inhabitants of leaf pouches and other specialized structures in plants known as myrmecophytes. However, the cues used by ant queens to locate suitable host-plants following dispersal remain poorly understood. Here we tested the hypothesis that Pheidole minutula queens use volatiles to distinguish their host Maieta guianensis (Melastomataceae) from other sympatric myrmecophytes. To do so, we used a Y-tube olfactometer to quantify the preference for volatiles of different plant species. Our results indicate that P. minutula queens discriminate the chemical volatiles produced by its host-plant from those of other sympatric ant-plant species. However, queens failed to distinguish the volatiles of Maieta from those of the ant-plant Tococa bullifera (Melastomataceae), with which P. minutula is not mutualistically associated. Nevertheless, a strong preference for Maieta over Tococa was observed during a subsequent bioassay, where the ants had physical contact with a domatium of each plant species. These results suggest that additional, short distance mechanisms are also necessary for host discrimination. Overall, our findings suggest that the high degree of compartmentalization observed in symbiotic ant–plant relationships is achieved, at least in part, by the relatively high degree of specificity in host selection displayed by foundress queens.     

Interspecific variation in the defensive responses of ant mutualists to plant volatiles

In ant–plant mutualist systems, ants patrol their host plants and search for herbivores. Such patrolling can be inefficient, however, because herbivore activity is spatio-temporally unpredictable. It has been proposed that rapid and efficient systems of communication between ants and plants, such as volatile compounds released following herbivory, both elicit defensive responses and direct workers to sites of herbivore activity. We performed bioassays in which we challenged colonies of two Amazonian plant-ants, Azteca sp. and Pheidole minutula , with extracts of leaf tissue from (1) their respective host-plant species ( Tococa bullifera and Maieta guianensis , both Melastomataceae), (2) sympatric ant-plants from the Melastomataceae, and (3) two sympatric but non-myrmecophytic Melastomataceae. We found that ants of both species responded dramatically to host-plant extracts, and that these responses are greater than those to sympatric myrmecophytes. Azteca sp. also responded to non-myrmecophytes with an intensity similar to that of sympatric ant-plants. By contrast, the response of P. minutula to any non-myrmecophytic extracts was limited. These differences may be driven in part by interspecific differences in nesting behaviour; although P. minutula only nests in host plants, Azteca sp. will establish carton satellite nests on nearby plants. We hypothesize that Azteca sp. must therefore recognize and defend a wider array of species than P. minutula .  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 94 , 241–249.     

Are myrmecophytes always better protected against herbivores than other plants?

The present field study compared the degree of defoliation of three Guianian melastome, two myrmecophytes (i.e. plants sheltering ants in hollow structures) and Clidemia sp., a nonmyrmecophytic plant serving as a control. Maieta guianensis Aubl. hosted mostly Pheidole minutula Mayr whatever the area, whereas Tococa guianensis Aubl. hosted mostly Azteca bequaerti Wheeler along streams and Crematogaster laevis Mayr or Azteca sp. 1 in the understory where it never blossomed. Only Tococa , when sheltering A. bequaerti in what can be considered as a truly mutualistic relationship, showed significantly less defoliation than control plants. In the other associations, the difference was not significant, but P. minutula is mutualistic with Maieta because it furnishes some protection (exclusion experiments) plus nutrients (previous studies). When devoid of ants, Tococa showed significantly greater defoliation than control plants; therefore, it was deduced that Tococa probably lacks certain antidefoliator metabolites that control plants possess (both Tococa and control plants are protected by ground-nesting, plant-foraging ants, which is termed 'general myrmecological protection'). Consequently, plant-ants other than A. bequaerti probably also protect Tococa slightly, thus compensating for this deficiency and permitting it to live in the understory until treefall gaps provide the conditions necessary for seed production.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 89 , 91–98.     

Herbivory and assemblage structure of myrmecophytous understory plants and their associated ants in the central Amazon

Summary The species combinations of myrmecophytic plants were compared in three different, neighboring local central Amazon forest sites. The proportional contribution of myrmecophytes in each setting varied significantly, withMaieta guainensis being the most abundant in each locality. This pattern resulted in low site similarity values. Other recorded species wereHirtella physophora, Tachigalia myrmecophila, Duroia sp.,Tococa sp., andCordia nodosa. Little variability was found with respect to associated ants that inhabited the myrmecophytes, and mutual entropies indicated a high degree of mutualistic interactions. However, for the majority of myrmecophytes, no differences in herbivore damage levels could be attributed to the presence of ants, with onlyM. guianensis andT. myrmecophila demonstrating significantly lower damages when inhabited by ants. Their respective ant associates,Pheidole minitula andPseudomyrmex concolor, were thus the only plant-ants with a demonstrable ability to reduce the levels of herbivory in their host plant.     

Mutualism between Maieta guianensis Aubl., a myrmecophytic melastome,and one of its ant inhabitants: ant protection against insect herbivores

Summary The hypothesis that ants (Pheidole minutula) associated with the myrmecophytic melastome Maieta guianensis defend their host-plant against herbivores was investigated in a site near Manaus, Amazonas, Brazil. M. guianensis is a small shrub that produces leaf pouches as ant domatia. Plants whose ants were experimentally removed suffered a significant increase in leaf damage compared with control plants (ants maintained). Ants patrol the young and mature leaves of Maieta with the same intensity, presumably since leaves of both ages are equally susceptible to herbivore attack. The elimination of the associated ant colony, and consequent increase in herbivory, resulted in reduced plant fitness. Fruit production was 45 times greater in plants with ants than in plants without ants 1 year after ant removal.     

Plant growth-altering effects of Azospirillum brasilense and Bacillus C–11–25 on two wheat cultivars

The effect of Azospirillum brasilense Cd, Bacillus C–11–25, indole acetic acid, gibberellic acid and cytokinin on plant growth characteristics of two wheat ( Triticum aestivum L. emend Thell) cultivars was studied under laboratory and greenhouse conditions. Responses of wheat plants to bacterial inoculation were similar to those caused by the addition of gibberellic acid in growth pouches. Chester and Fielder wheat varieties differed in responses to the bacteria and hormone additions. When added to growth pouches, bacterial culture filtrates and dead bacterial cells caused plant growth responses similar to those caused by the addition of live cells. Bacteria and hormone additions resulted in increased permeability of Fielder wheat to ¹⁵Nlabelled nitrate, and decreased nitrate permeability of Chester wheat. Bacterial inoculation of soil in pots caused ¹⁵N isotope dilution in Fielder but not in Chester wheat. Hormone addition to pots caused isotope dilution in Chester wheat. It appeared that genetic differences between cultivars affected plant growth responses. The accuracy of estimates of N₂ fixation by associative bacteria based on ¹⁵N isotope dilution calculations may be reduced if control plants differ in plant response to these bacteria.     

Predation Success By A Plant-Ant Indirectly Favours The Growth And Fitness Of Its Host Myrmecophyte

Mutualisms, or interactions between species that lead to net fitness benefits for each species involved, are stable and ubiquitous in nature mostly due to “byproduct benefits” stemming from the intrinsic traits of one partner that generate an indirect and positive outcome for the other. Here we verify if myrmecotrophy (where plants obtain nutrients from the refuse of their associated ants) can explain the stability of the tripartite association between the myrmecophyte Hirtella physophora, the ant Allomerus decemarticulatus and an Ascomycota fungus. The plant shelters and provides the ants with extrafloral nectar. The ants protect the plant from herbivores and integrate the fungus into the construction of a trap that they use to capture prey; they also provide the fungus and their host plant with nutrients. During a 9-month field study, we over-provisioned experimental ant colonies with insects, enhancing colony fitness (i.e., more winged females were produced). The rate of partial castration of the host plant, previously demonstrated, was not influenced by the experiment. Experimental plants showed higher δ¹⁵N values (confirming myrmecotrophy), plus enhanced vegetative growth (e.g., more leaves produced increased the possibility of lodging ants in leaf pouches) and fitness (i.e., more fruits produced and more flowers that matured into fruit). This study highlights the importance of myrmecotrophy on host plant fitness and the stability of ant-myrmecophyte mutualisms.     

Host‐plant use by two Orthomeria (Phasmida: Aschiphasmatini) species feeding on Macaranga myrmecophytes

Myrmecophytes depend on symbiotic ants (plant‐ants) to defend against herbivores. Although these defensive mechanisms are highly effective, some herbivorous insects can use myrmecophytes as their host‐plants. The feeding habits of these phytophages on myrmecophytes and the impacts of the plant‐ants on their feeding behavior have been poorly studied. We examined two phasmid species, Orthomeria alexis and O. cuprinus, which are known to feed on Macaranga (Euphorbiaceae) myrmecophytes in a Bornean primary forest. Our observations revealed that: (i) each phasmid species relied on two closely‐related myrmecophytic Macaranga species for its host‐plants in spite of their normal plant‐ant symbioses; and (ii) there was little overlap between their host‐plant preferences. More O. cuprinus adults and nymphs were found on new leaves, which were attended by more plant‐ants than mature leaves, while most adults and nymphs of O. alexis tended to avoid new leaves. In a feeding choice experiment under ant‐excluded conditions, O. alexis adults chose a non‐host Macaranga myrmecophyte that was more intensively defended by plant‐ants and was more palatable than their usual host‐plants almost as frequently as their usual host‐plant, suggesting that the host‐plant range of O. alexis was restricted by the presence of plant‐ants on non‐host‐plants. Phasmid behavior that appeared to minimize plant‐ant attacks is described.     

Elucidating the nutritional dynamics of fungi using stable isotopes

Mycorrhizal and saprotrophic (SAP) fungi are essential to terrestrial element cycling due to their uptake of mineral nutrients and decomposition of detritus. Linking these ecological roles to specific fungi is necessary to improve our understanding of global nutrient cycling, fungal ecophysiology, and forest ecology. Using discriminant analyses of nitrogen (δ¹⁵N) and carbon (δ¹³C) isotope values from 813 fungi across 23 sites, we verified collector-based categorizations as either ectomycorrhizal (ECM) or SAP in > 91% of the fungi, and provided probabilistic assignments for an additional 27 fungi of unknown ecological role. As sites ranged from boreal tundra to tropical rainforest, we were able to show that fungal δ¹³C (26 sites) and δ¹⁵N (32 sites) values could be predicted by climate or latitude as previously shown in plant and soil analyses. Fungal δ¹³C values are likely reflecting differences in C-source between ECM and SAP fungi, whereas ¹⁵N enrichment of ECM fungi relative to SAP fungi suggests that ECM fungi are consistently delivering ¹⁵N depleted N to host trees across a range of ecosystem types.     

An Assassin among Predators: The Relationship between Plant-Ants,Their Host Myrmecophytes and the Reduviidae Zelus annulosus

Tropical plants frequently live in association with ants that protect their foliage from defoliators. Among them, myrmecophytes have evolved mutualisms with a limited number of plant-ants that they shelter and feed, and, in return, benefit from some protection. Hirtella physophora (Chrysobalanaceae), for example, houses Allomerus decemarticulatus (Myrmicinae) that build gallery-shaped traps to catch large prey. In French Guiana, we frequently observed the assassin bug Zelus annulosus (Reduviidae, Harpactorinae) on the leaves of H. physophora. Here, we studied the distribution of Zelus annulosus among understory plants in the Guianese rainforest and found it only on pubescent plants, including H. Physophora, whether or not it was sheltering an A. decemarticulatus colony, but only rarely on other myrmecophytes. The relationship between Z. annulosus and its host plants is, then, also mutualistic, as the plant trichomes act as an enemy-free space protecting the nymphs from large predatory ants, while the nymphs protect their host-plants from herbivorous insects. Through their relationship with A. decemarticulatus colonies, Z. annulosus individuals are protected from army ants, while furnishing nothing in return. In those cases where H. physophora sheltered both an A. decemarticulatus colony and Z. annulosus nymphs, certain plant individuals repeatedly sheltered nymphs, indicating that female bugs may select not only pubescent plants but also particular H. physophora treelets having characteristics more favourable to the development of their progeny.     

Dynamics of the association between a long-lived understory myrmecophyte and its specific associated ants

Myrmecophytic symbioses are widespread in tropical ecosystems and their diversity makes them useful tools for understanding the origin and evolution of mutualisms. Obligate ant–plants, or myrmecophytes, provide a nesting place, and, often, food to a limited number of plant–ant species. In exchange, plant–ants protect their host plants from herbivores, competitors and pathogens, and can provide them with nutrients. Although most studies to date have highlighted a similar global pattern of interactions in these systems, little is known about the temporal structuring and dynamics of most of these associations. In this study we focused on the association between the understory myrmecophyte Hirtella physophora (Chrysobalanaceae) and its obligate ant partner Allomerus decemarticulatus (Myrmicinae). An examination of the life histories and growth rates of both partners demonstrated that this plant species has a much longer lifespan (up to about 350 years) than its associated ant colonies (up to about 21 years). The size of the ant colonies and their reproductive success were strongly limited by the available nesting space provided by the host plants. Moreover, the resident ants positively affected the vegetative growth of their host plant, but had a negative effect on its reproduction by reducing the number of flowers and fruits by more than 50%. Altogether our results are important to understanding the evolutionary dynamics of ant–plant symbioses. The highly specialized interaction between long-lived plants and ants with a shorter lifespan produces an asymmetry in the evolutionary rates of the interaction which, in return, can affect the degree to which the interests of the two partners converge.     

Ant species confer different partner benefits on two neotropical myrmecophytes

The dynamics of mutualistic interactions involving more than a single pair of species depend on the relative costs and benefits of interaction among alternative partners. The neotropical myrmecophytes Cordia nodosa and Duroia hirsuta associate with several species of obligately symbiotic ants. I compared the ant partners of Cordia and Duroia with respect to two benefits known to be important in ant-myrmecophyte interactions: protection against herbivores provided by ants, and protection against encroaching vegetation provided by ants. Azteca spp., Myrmelachista schumanni, and Allomerus octoarticulatus demerarae ants all provide the leaves of Cordia and Duroia some protection against herbivores. However, Azteca and Allomerus provide more protection than does Myrmelachista to the leaves of their host plants. Although Allomerus protects the leaves of its hosts, plants occupied by Allomerus suffer more attacks by herbivores to their stems than do plants occupied by other ants. Relative to Azteca or Allomerus, Myrmelachista ants provide better protection against encroaching vegetation, increasing canopy openness over their host plants. These differences in benefits among the ant partners of Cordia and Duroia are reflected in the effect of each ant species on host plant size, growth rate, and reproduction. The results of this study show how mutualistic ant partners can differ with respect to both the magnitude and type of benefits they provide to the same species of myrmecophytic host.     

CAM-cycling in the cycad Dioon edule Lindl. in its natural tropical deciduous forest habitat in central Veracruz, Mexico

The cycad Dioon edule Lindl. inhabits a seasonally-dry tropical forest along with associated CAM plants such as bromeliads and cacti. To test the hypothesis that D . edule might also be a CAM plant, diel total-acid fluctuation was measured through the dry to wet seasons of 4 consecutive years on adult D . edule plants in their natural forest habitat in Veracruz, Mexico. Correlations between acid fluctuation index and climatic data, and also soil water potential were determined over this period. Laboratory trials were followed up to estimate diel patterns of CO₂ exchange and estimation of δ¹³C value. A comparison of stomatal density cm⁻² with other C₃, CAM and CAM-facultative plants was made. The diel total titratable-acid fluctuation values, although variable, were found to be consistent and significant for the dry season. Carbon dioxide exchange was found to be typical of C₃ plants when hydrated but when the plant was stressed by withholding water, although the leaf remained healthy, there was no significant dark-period CO₂ output. Stomatal density was comparable to other CAM and CAM-facultative plants. It was concluded that D. edule is a C₃ plant that shows CAM-cycling metabolism when water stressed. © 2002 The Linnean Society of London, Botanical Journal of the Linnean Society , 138 , 155–161.     

Induced biotic responses to herbivory and associated cues in the Amazonian ant-plant Maieta poeppigii

Ants inhabiting ant‐plants can respond to cues of herbivory, such as the presence of herbivores, leaf damage, and plant sap, but experimental attempts to quantify the dynamic nature of biotic defenses have been restricted to a few associations between plants and ants. We studied the relationship between certain features of the ant‐shrub Maieta poeppigii Cogn. (Melastomataceae) and the presence or absence of ant patrolling on the leaf surface in plants occupied by the ant Pheidole minutula Mayr (Hymenoptera: Formicidae). We also carried out field experiments to examine ant behavior following plant damage, and the potential cues that induce ant recruitment. These experiments included clipping of the leaf apex, as well as the presentation of a potential herbivore (live termite worker) and a foliar extract from Maieta on treatment leaves. The presence of ants patrolling the leaves of M. poeppigii is influenced by the number of domatia on the plant. Ant patrolling on the leaves of M. poeppigii was constant throughout a 24 h cycle, but the mean number of patrolling ants decreased from young to mature leaves, and from leaves with domatia to those without domatia. There was an overall increase in the number of ants on experimental leaves following all treatments, compared to control leaves. Visual and chemical cues associated with herbivory are involved in the induction of ant recruitment in the Maieta–Pheidole system. The continuous patrolling behavior of ants, associated with their ability to respond rapidly to foliar damage, may result in the detection and repellence/capture of most insect herbivores before they can inflict significant damage to the leaves.     

Bulk leaf δ18O and δ13C reflect the intensity of intraspecific competition for water in a semi-arid tussock grassland

We investigated the extent to which plant water and nutrient status are affected by intraspecific competition intensity and microsite quality in a monodominant tussock grassland. Leaf gas exchange and stable isotope measurements were used to assess the water relations of Stipa tenacissima tussocks growing along a gradient of plant cover and soil depth in a semi-arid catchment of Southeast Spain. Stomatal conductance and photosynthetic rate decreased with increasing intensity of competition during the wet growing season, leading to foliar δ ¹⁸O and δ ¹³C enrichment. A high potential for runoff interception by upslope neighbours exerted strong detrimental effects on the water and phosphorus status of downslope S. tenacissima tussocks. Foliar δ ¹⁵N values became more enriched with increasing soil depth. Multiple stepwise regression showed that competition potential and/or rhizosphere soil depth accounted for large proportions of variance in foliar δ ¹³C, δ ¹⁸O and δ ¹⁵N among target tussocks (57, 37 and 64%, respectively). The results presented here highlight the key role that spatial redistribution of resources (water and nutrients) by runoff plays in semi-arid ecosystems. It is concluded that combined measurement of δ ¹³C, δ ¹⁸O and nutrient concentrations in bulk leaf tissue can provide insight into the intensity of competitive interactions occurring in natural plant communities.     

Ant-Repelling Pollinators of the Myrmecophytic <Emphasis Type="Italic">Macaranga winkleri</Emphasis> (Euphorbiaceae)

Many plants have mutualistic relationships with ants, whereby plants provide food and/or nesting sites for the symbiotic ants, and in turn the ants protect the host plants by excluding herbivores. While the ants are useful as guards, they may negatively affect host reproduction by excluding pollinators. Here we studied this potential conflict in the myrmecophytic Macaranga winkleri pollinated by the thrips Dolichothrips fialae. Behavioural responses of ant guards to pollinator thrips and their chemicals, and related chemical analyses, provide evidence that thrips deter ant-guards by secreting droplets containing ant-repelling n-decanoic acid from their anuses. This is the first report of insect pollinators repelling their host’s symbiotic guard ants to perform pollination. This is a novel strategy by which a plant host avoids interference with pollination by ant-guards in an ant–plant mutualism. The acquisition of a pollination system that is resistant to ant attacks may have facilitated the evolution of myrmecophytes in the genus Macaranga.     

Studies of a South East Asian ant-plant association: protection of Macaranga trees by Crematogaster borneensis

Summary In the humid tropics of SE Asia there are some 14 myrmecophytic species of the pioneer tree genus Macaranga (Euphorbiaceae). In Peninsular Malaysia a close association exists between the trees and the small, non-stinging myrmicine Crematogaster borneensis. These ants feed mainly on food bodies provided by the plants and have their colonies inside the hollow internodes. In a ten months field study we were able to demonstrate for four Macaranga species (M. triloba, M. hypoleuca, M. hosei, M. hulletti) that host plants also benefit considerably from ant-occupation. Ants do not contribute to the nutrient demands of their host plant, they do, however, protect it against herbivores and plant competition. Cleaning behaviour of the ants results in the removal of potential hervivores already in their earliest developmental stages. Strong aggressiveness and a mass recruiting system enable the ants to defend the host plant against many herbivorous insects. This results in a significant decrease in leaf damage due to herbivores on ant-occupied compared to ant-free myrmecophytes as well as compared to non-myrmecophytic Macaranga species. Most important is the ants' defense of the host plant against plant competitors, especially vines, which are abundant in the well-lit pioneer habitats where Macaranga grows. Ants bite off any foreign plant part coming into contact with their host plant. Both ant-free myrmecophytes and non-myrmecophytic Macaranga species had a significantly higher incidence of vine growth than specimens with active ant colonies. This may be a factor of considerable importance allowing Macaranga plants to grow at sites of strongest competition.     

Mechanisms driving the specificity of a myrmecophyte–ant association

In the understory of pristine Guianese forests, the myrmecophyte Hirtella physophora almost exclusively shelters colonies of the plant-ant Allomerus decemarticulatus in its leaf pouches. We experimentally tested three non-mutually exclusive hypotheses concerning phenomena that can determine the species specificity of this association throughout the foundation stage of the colonies: (1) interspecific competition results in the overwhelming presence of A. decemarticulatus queens or incipient colonies; (2) exclusion filters prevent other ant species from entering the leaf pouches; and (3) host-recognition influences the choice of founding queens, especially A. decemarticulatus . Neither interspecific competition, nor the purported exclusion filters that we examined play a major role in maintaining the specificity of this association. Unexpectedly, the plant trichomes lining the domatia appear to serve as construction material during claustral foundation rather than as a filter. Finally, A. decemarticulatus queens are able to identify their host plant from a distance through chemical and/or visual cues, which is rarely demonstrated in studies on obligatory ant–plant associations. We discuss the possibility that this specific host-recognition ability could participate in shaping a compartmentalized plant-ant community where direct competition between ant symbionts is limited.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 97 , 90–97.     

Stem diversity, cauline domatia, and the evolution of ant-plant associations in Piper sect. Macrostachys (Piperaceae)

Plants possess a variety of structures that harbor ant nests, and the morphology of these domatia determines the nature of ant-plant mutualisms in a given plant species. In this study, we report on the differences in anatomy between myrmecophytes of Piper, which are regularly excavated by an obligate ant mutualist (Pheidole bicornis) and nonmyrmecophytes of Piper, which consistently have solid stems. Stems of excavated plant species lacked outward evidence of modification; however, striking anatomical differences were apparent between hollow-stemmed species before excavation and the remainder of the solid-stemmed species studied. Prior to excavation by ants, stems of myrmecophytes were characterized by strongly heterogeneous piths in which a large, central area had relatively large cells lacking intracellular crystals with a periphery of smaller cells containing numerous crystals. The domatium excavated by the ants was restricted to the large-celled region. This is the first report of the absence of crystals in ant-excavated portions of stems of myrmecophytes. Cauline domatia became lined with 3-8 cell layers of suberized wound tissue, which may have an impact on nutrient absorption by Piper myrmecophytes.     

Oxygen isotope enrichment (Δ18O) reflects yield potential and drought resistance in maize

Measurement of stable isotopes in plant dry matter is a useful phenotypic tool for speeding up breeding advance in C₃ crops exposed to different water regimes. However, the situation in C₄ crops is far from resolved, since their photosynthetic metabolism precludes (at least in maize) the use of carbon isotope discrimination. This paper investigates the use of oxygen isotope enrichment (Δ¹⁸O) as a new secondary trait for yield potential and drought resistance in maize ( Zea mays L). A set of tropical maize hybrids developed by the International Maize and Wheat Improvement Center was grown under three contrasting water regimes in field conditions. Water regimes clearly affected plant growth and yield. In accordance with the current theory, a decrease in water input was translated into large decreases in stomatal conductance and increases in leaf temperature together with concomitant ¹⁸O enrichment of plant matter (leaves and kernels). In addition, kernel Δ¹⁸O correlated negatively with grain yield under well-watered and intermediate water stress conditions, while it correlated positively under severe water stress conditions. Therefore, genotypes showing lower kernel Δ¹⁸O under well-watered and intermediate water stress had higher yields in these environments, while the opposite trend was found under severe water stress conditions. This illustrates the usefulness of Δ¹⁸O for selecting the genotypes best suited to differing water conditions.