Timescales of population rarity and commonness in random environments

This is a mathematical study of the interactions between non-linear feedback (density dependence) and uncorrelated random noise in the dynamics of unstructured populations. The stochastic non-linear dynamics are generally complex, even when the deterministic skeleton possesses a stable equilibrium. There are three critical factors of the stochastic non-linear dynamics; whether the intrinsic population growth rate (lambda) is smaller than, equal to, or greater than 1; the pattern of density dependence at very low and very high densities; and whether the noise distribution has exponential moments or not. If lambda < 1, the population process is generally transient with escape towards extinction. When lambda > or = 1, our quantitative analysis of stochastic non-linear dynamics focuses on characterizing the time spent by the population at very low density (rarity), or at high abundance (commonness), or in extreme states (rarity or commonness). When lambda >1 and density dependence is strong at high density, the population process is recurrent: any range of density is reached (almost surely) in finite time. The law of time to escape from extremes has a heavy, polynomial tail that we compute precisely, which contrasts with the thin tail of the laws of rarity and commonness. Thus, even when lambda is close to one, the population will persistently experience wide fluctuations between states of rarity and commonness. When lambda = 1 and density dependence is weak at low density, rarity follows a universal power law with exponent -3/2. We provide some mathematical support for the numerical conjecture [Ferriere, R., Cazelles, B., 1999. Universal power laws govern intermittent rarity in communities of interacting species. Ecology 80, 1505-1521.] that the -3/2 power law generally approximates the law of rarity of 'weakly invading' species with lambda values close to one. Some preliminary results for the dynamics of multispecific systems are presented.     

Rarity and persistence

Rarity is a population characteristic that is usually associated with a high risk of extinction. We argue here, however, that chronically rare species (those with low population densities over many generations across their entire ranges) may have individual‐level traits that make populations more resistant to extinction. The major obstacle to persistence at low density is successful fertilisation (union between egg and sperm), and chronically rare species are more likely to survive when (1) fertilisation occurs inside or close to an adult, (2) mate choice involves long‐distance signals, (3) adults or their surrogate gamete dispersers are highly mobile, or (4) the two sexes are combined in a single individual. In contrast, external fertilisation and wind‐ or water‐driven passive dispersal of gametes, or sluggish or sedentary adult life habits in the absence of gamete vectors, appear to be incompatible with sustained rarity. We suggest that the documented increase in frequency of these traits among marine genera over geological time could explain observed secular decreases in rates of background extinction. Unanswered questions remain about how common chronic rarity actually is, which traits are consistently associated with chronic rarity, and how chronically rare species are distributed among taxa, and among the world's ecosystems and regions.     

Limits to the abundance of rare species: an experimental test with a tree aphid

Abstract. 1. The birch ( Betula )-feeding aphid, Monaphis antennata, is always found at low densities on individual hosts and has low local abundance, but another birch-feeding aphid, Euceraphis betulae , is often found at high densities on individual hosts and has high local abundance.
2. This work attempts to establish whether the interaction between M. antennata and its host or the behaviour of individuals limits its densities.
3. Both species were reared on saplings, and population sizes were monitored for 6 weeks. Two levels of host quality were used and feeding space was kept constant throughout the experiment. Adults were prevented from leaving the saplings by clipping their wings, and predators were excluded.
4. On plants of similar host quality, both species achieved similar population sizes.
5. It is concluded that resource availability or the interactions between individuals are unlikely to be important causes of rarity.     

Rarity within taxonomie lineages and the use of taxa above the level of species

Studies which attempt to explain rarity lineages are becoming increasingly popular. An ability to explain causative factors for rarity based on shared characteristics in an intuitively attractive concept, since it may greatly reduce the number of studies needed to understand rarity in all species. Most studies have used the taxonomic unit of family as the level at which patterns in the distribution of rarity re examined, though no justification for the use of family has been provided. To date, No evidence has been produced to show that family-based patterns represent patterns at lower taxonomic levels.
To test whether family-based levels of rarity reliably reflected generic levels. J compared the incidence of rarity within 114 genera from 47 families, 113 genera (<99%) within 46 families showed no difference from family means in the proportion of rare species they contained, indicating that the incidence of rarity is consistent between the taxonomic levels of family and genus. This result suggests family level patterns reflect pattern at lower taxonomic levels and supports the use of family as an appropriate level to investigate patterns in the distribution of rarity within a flora     

Use of arthropod rarity for area prioritisation: insights from the Azorean Islands

We investigated the conservation concern of Azorean forest fragments and the entire Terceira Island surface using arthropod species vulnerability as defined by the Kattan index, which is based on species rarity. Species rarity was evaluated according to geographical distribution (endemic vs. non endemic species), habitat specialization (distribution across biotopes) and population size (individuals collected in standardized samples). Geographical rarity was considered at 'global' scale (species endemic to the Azorean islands) and 'regional' scale (single island endemics). Measures of species vulnerability were combined into two indices of conservation concern for each forest fragment: (1) the Biodiversity Conservation Concern index, BCC, which reflects the average rarity score of the species present in a site, and (2) one proposed here and termed Biodiversity Conservation Weight, BCW, which reflects the sum of rarity scores of the same species assemblage. BCW was preferable to prioritise the areas with highest number of vulnerable species, whereas BCC helped the identification of areas with few, but highly threatened species due to a combination of different types of rarity.A novel approach is introduced in which BCC and BCW indices were also adapted to deal with probabilities of occurrence instead of presence/absence data. The new probabilistic indices, termed pBCC and pBCW, were applied to Terceira Island for which we modelled species distributions to reconstruct species occurrence with different degree of probability also in areas from which data were not available. The application of the probabilistic indices revealed that some island sectors occupied by secondary vegetation, and hence not included in the current set of protected areas, may in fact host some rare species. This result suggests that protecting marginal non-natural areas which are however reservoirs of vulnerable species may also be important, especially when areas with well preserved primary habitats are scarce.     

Analysis of the factors that affect the distribution and abundance of three Neobuxbaumia species (Cactaceae) that differ in their degree of rarity

We studied three species of columnar cacti in the genus Neobuxbaumia which differ in their degree of rarity: Neobuxbaumia macrocephala (the rarest), Neobuxbaumia tetetzo (intermediate), and Neobuxbaumia mezcalaensis (the most common). To investigate the ecological factors that limit their distribution and abundance, we surveyed 80 localities within the region of Tehuacan-Cuicatlán, in Central Mexico. At each locality we measured several environmental variables, and the density of the Neobuxbaumia populations present. We used a principal component analysis (PCA) to identify the factors that are associated to the presence/absence of each species. Additionally, we carried out multiple regressions between environmental variables and population density to test whether the variation in these variables was related to changes in abundance. The results show that factors significantly affecting the distribution of these species are mean annual temperature, altitude, rainfall, and soil properties such as texture and organic matter content. N. mezcalaensis reaches maximum population densities of 14,740 plants per ha (average density = 3943 plants per ha) and is associated with localities with relatively abundant rainfall. N. tetetzo shows maximum population densities of 14,060 plants per ha (average = 3070 plants per ha), and is associated with sites located at high latitudes and with high phosphorous content in the soil. The rarest species, N. macrocephala, shows maximum densities of 1180 plants per ha (average = 607 plants per ha) and is associated with localities with high soil calcium content. The distribution of this species is limited to sites with specific values of the environmental variables recorded, conferring it a high habitat specificity which accounts for its rarity.     

Ecological implications of the relative rarity of fossil hominins at Laetoli

Hominins are a very rare component of the large-mammal fauna at Laetoli. Although no equivalent data are available for Hadar, the much higher count and relative abundance of hominins suggests that they may have been more common at the latter site. The apparent relative rarity of hominins at Laetoli may have significant implications for understanding the ecology of Australopithecus afarensis. However, it is essential to first assess the extent to which taphonomic variables might have been a contributing factor. Using data from fossil ruminants, we show that the survivability of skeletal elements at Laetoli relates to the extent to which they can resist carnivore scavenging and their likelihood of being entirely buried by volcanic ashes and tuffaceous sediments. The rarity of hominins at Laetoli is probably due in part to the influence of these two taphonomic factors. However, these factors cannot account entirely for the difference in hominin relative abundance between these two sites, and ecological differences were probably a contributing factor. The highest population densities of chimpanzees today occur in forest and closed woodland, with reduced densities in open woodland. If similar levels of population-density variation characterized A. afarensis, the differences between Hadar and Laetoli may relate to the quality/optimality of the habitats. Hadar was, in general, much more densely wooded and mesic than Laetoli, with permanent and substantial bodies of water. In contrast, Laetoli was predominantly a woodland-shrubland-grassland mosaic supported only by ephemeral streams and ponds. The apparent greater relative abundance of hominins at Hadar compared with Laetoli suggests that, like chimpanzees, A. afarensis may have been more successful in more densely wooded habitats. Compared with Hadar, Laetoli probably represented a less optimal habitat for the foraging and dietary behavior of A. afarensis, and this is reflected in their inferred lower abundance, density, and biomass.     

Plant Trait-Species Abundance Relationships Vary with Environmental Properties in Subtropical Forests in Eastern China

Understanding how plant trait-species abundance relationships change with a range of single and multivariate environmental properties is crucial for explaining species abundance and rarity. In this study, the abundance of 94 woody plant species was examined and related to 15 plant leaf and wood traits at both local and landscape scales involving 31 plots in subtropical forests in eastern China. Further, plant trait-species abundance relationships were related to a range of single and multivariate (PCA axes) environmental properties such as air humidity, soil moisture content, soil temperature, soil pH, and soil organic matter, nitrogen (N) and phosphorus (P) contents. At the landscape scale, plant maximum height, and twig and stem wood densities were positively correlated, whereas mean leaf area (MLA), leaf N concentration (LN), and total leaf area per twig size (TLA) were negatively correlated with species abundance. At the plot scale, plant maximum height, leaf and twig dry matter contents, twig and stem wood densities were positively correlated, but MLA, specific leaf area, LN, leaf P concentration and TLA were negatively correlated with species abundance. Plant trait-species abundance relationships shifted over the range of seven single environmental properties and along multivariate environmental axes in a similar way. In conclusion, strong relationships between plant traits and species abundance existed among and within communities. Significant shifts in plant trait-species abundance relationships in a range of environmental properties suggest strong environmental filtering processes that influence species abundance and rarity in the studied subtropical forests.     

Changes in rain forest tree diversity, dominance and rarity across a seasonality gradient in the Western Ghats, India

Aim We assessed the effects of latitude, altitude and climate on the alpha diversity of rain forest trees in the Western Ghats (WG) of India. We tested whether stem densities, dominance, the prevalence of rarity, and the proportion of understorey trees are significantly correlated with alpha diversity. Location The WG is a chain of mountains c. 1600 km in length, running parallel to the western coast of the Indian peninsula from above 8° N to almost 21° N latitude. Wet forests occur as a narrow strip in regions with heavy rainfall. Methods To assess tree diversity we used data from 40 small plots, < 1 ha in area, where all trees ≥ 3.18 cm d.b.h. had been inventoried. These plots were distributed across 7 latitudinal degrees and at elevations between 200 and 1550 m. Fisher's alpha was used as a measure of diversity. For each plot, the proportion of trees belonging to the understorey, the proportion of trees belonging to the most abundant species in the plot, as a measure of dominance, and the proportionate representation of singletons, as a measure of rarity, were estimated, and correlated with Fisher's alpha, elevation, rainfall and seasonality. Results Annual rainfall and seasonality increased towards the north, but were not significantly correlated. Tree diversity increased significantly with decreasing seasonality. Tree diversity was not significantly correlated with stem density or with the proportion of understorey tree species, but was significantly correlated with tree dominance and rarity. Dominance increased and rarity significantly decreased with increasing seasonality. Main conclusions This study demonstrates that seasonality influences rain forest tree diversity in the WG of India. The relationship between alpha diversity, dominance and rarity lends correlative support for the Janzen–Connell pest pressure hypothesis.     

Cross-taxon congruence in the rarity of subtidal rocky marine assemblages: No taxonomic shortcut for conservation monitoring

The implementation of protection strategies such as the European Marine Strategy Framework Directive (2008/56/EC) is impeded for subtidal rock bottom habitats because of high sampling costs due to a very wide taxonomic diversity, and a lack of suitable evaluation tools to estimate their conservation importance. In this study, we seek to provide an evaluation procedure by (1) investigating the distribution of rarity among subtidal rock bottom phyla; (2) searching for potential surrogate phyla with a cross-taxon congruence approach based on their rarity; (3) proposing an appropriate multi-phyla indicator to evaluate the importance of subtidal rocky habitats for conservation. We analysed the distribution of 548 species belonging to 8 phyla sampled in 137 assemblages in subtidal rocky areas located around Brittany, Western France. We applied the Index of Relative Rarity, a flexible method which fits rarity weights to species depending on their respective phyla. We found only weak congruence in rarity patterns among phyla, which prevented any attempt to identify surrogate phyla. This finding has important implications for the conservation of subtidal rocky habitats as it means that there is no shortcut to monitor their rarity: working on a subset of phyla would imply a biased evaluation of biodiversity. Consequently, we propose a multi-phyla Index of Relative Rarity combining all phyla which allowed us to successfully describe rarity patterns across all sampled sites.     

Inbreeding in Littledale's whistling rat Parotomys littledalei

Despite its rarity in nature, inbreeding is sometimes evident in species occupying ephemeral, unpredictable habitats, and which occur at low densities. One such species is Littledale's whistling rat, Parotomys littledalei, a murid rodent endemic to the south-west arid region of South Africa. Using a captive population of P. littledalei, I studied mate choice for kin and nonkin, and the reproductive performance of inbred and outbred pairs. In choice tests, estrous females presented with either odors or actual males showed a preference for siblings or half-siblings to unrelated males. Males did not discriminate between the odor of estrous kin and nonkin. In breeding studies, inbred (mother-son; brother-sister) and outbred (proven female and an unrelated young male and nonsiblings) pairs had a similar reproductive output, although the sex ratio favored males in inbred litters. The development of inbred young was indistinguishable from outbred young. The results indicate that female P. littledalei prefer to inbreed, but there are no apparent advantages to inbreeding over outbreeding.     

Multiple measures are necessary to assess rarity in macro-molluscs: a case study from southeastern Australia

Our knowledge of suitable criteria to determine rarity in most marine invertebrates is lacking, thus hindering targeted impact studies, long-term monitoring programs, and associated conservation strategies. Standardized definitions of rarity are required to enable comparisons of different assemblages and taxa. Gaston (Rarity, Chapman and Hall, Melbourne, 1994) has recommended that rare species are defined as the lowest quartile of species in the assemblage. In this study, the 25% ‘cut-off’ was applied to intertidal macro-molluscs along the Illawarra Coast, Australia from 200 surveys of 13 reefs, using three measures of population structure; (1) local abundance (numerical rarity); (2) number of locations (spatial rarity) and; (3) percent of surveys (temporal rarity). Rare species were consequently defined as those species with no more than; (1) a local abundance of two individuals; (2) a regional occurrence at two reefs and/or; (3) a temporal occurrence in 2% of all surveys. These cut-off values increased when only intertidal specialists were analysed. Using a combination of all three measures, 62 species (42%) were classified as regionally rare, but only four of these were true intertidal specialists. Most species were rare by only one or two definitions of rarity; illustrating the importance of considering multiple measures of rarity and the need to design specifically targeted survey methods for future monitoring. Many species that are rare by all three definitions are likely to be temporary immigrants, as subtidal species were significantly more likely to be classified as rare. Clearly many factors can influence the rarity of marine invertebrates on intertidal reefs, and these must all be considered to set appropriate conservation priorities.     

Functional rarity of plants in German hay meadows — Patterns on the species level and mismatches with community species richness

Functional rarity (FR) — a feature combining a species'' rarity with the distinctiveness of its traits — is a promising tool to better understand the ecological importance of rare species and consequently to protect functional diversity more efficiently. However, we lack a systematic understanding of FR on both the species level (which species are functionally rare and why) and the community level (how is FR associated with biodiversity and environmental conditions). Here, we quantify FR for 218 plant species from German hay meadows on a local, regional, and national scale by combining data from 6500 vegetation relevés and 15 ecologically relevant traits. We investigate the association between rarity and trait distinctiveness on different spatial scales via correlation measures and show which traits lead to low or high trait distinctiveness via distance‐based redundancy analysis. We test how species richness and FR are correlated, and use boosted regression trees to determine environmental conditions that are driving species richness and FR. On the local scale, only rare species showed high trait distinctiveness while on larger spatial scales rare and common species showed high trait distinctiveness. As infrequent trait attributes (e.g., legumes, low clonality) led to higher trait distinctiveness, we argue that functionally rare species are either specialists or transients. While specialists occupy a particular niche in hay meadows leading to lower rarity on larger spatial scales, transients display distinct but maladaptive traits resulting in high rarity across all spatial scales. More functionally rare species than expected by chance occurred in species‐poor communities indicating that they prefer environmental conditions differing from characteristic conditions of species‐rich hay meadows. Finally, we argue that functionally rare species are not necessarily relevant for nature conservation because many were transients from surrounding habitats. However, FR can facilitate our understanding of why species are rare in a habitat and under which conditions these species occur.     

The geographical distribution of rarity

Summary This paper asks the question: are most species that are censused as rare in particular localities rare throughout most of their geographic ranges, or are they common in substantial portions of their ranges elsewhere? The first alternative is labeled suffusive rarity and the second diffusive rarity. To answer this and similar questions, rarity can be measured as the fraction of censuses from some locality (e.g., a quadrat) in which a species occurs (occurrence rarity), or the relative or absolute abundance of the species averaged over all censuses from some locality (abundance rarity). The question was analyzed for occurrence-rarity data from Australian terrestrial birds distributed over 1° (10⁴-km²) quadrats. The great majority of species that are rare in a particular quadrat are not rare and are often common in a substantial number of other quadrats, i.e., these avian species are much closer to the diffusive than suffusive portion of the rarity continuum. The data also show that 1) the distribution of sizes of geographic ranges, whether breeding or total, is highly skewed, appearing exponential to more concave; 2) species are much rarer in their nonbreeding than breeding ranges; 3) more widespread species, whether breeding or total ranges are considered, tend to occur more rarely in a slightly but significantly greater fraction of their ranges; and 4) hawks and owls, typified by high abundance rarity, show occurrence rarity in a greater fraction of their ranges than the average nonraptorial species. Although continental birds may be especially predilected toward diffusive rarity, the present analysis points to identification of centers of abundance as major ways of preserving those species contributing most to recorded instances of rarity. Similar analyses with other kinds of organisms would be most welcome.     

Orchid biogeography and factors associated with rarity in a biodiversity hotspot,the Southwest Australian Floristic Region

Aim The causes of orchid diversification and intrinsic rarity are poorly resolved. The Orchidaceae of the Southwest Australian Floristic Region use a diversity of pollination strategies and sites of mycorrhizal infection, and occupy a diversity of habitats. We combined a biogeographic analysis with analysis of factors associated with rarity to establish: (1) the landscape features correlated with taxon turnover and speciation, and (2) the possible role in taxon rarity of geographic region, pollination strategy, edaphic habitat and site of mycorrhizal infection. Location Southwest Australian Floristic Region. Methods The distributions of 407 orchid taxa (species and subspecies) were mapped at the quarter‐degree scale using 13,267 collections in the Western Australian Herbarium. This database was used to map taxon richness, for a biogeographic analysis and to quantify rarity of taxa. Using herbarium records, rarity was expressed as mean abundance, mean distribution and incidence of rarity based on abundance and distribution for each genus. We tested for differences in rarity of species between pollination strategies, edaphic habitats and sites of mycorrhizal infection. Results Taxon richness was highest in the High Rainfall Province. Biogeographic provincial boundaries for orchids were aligned with rainfall, while district boundaries tended to follow geological formations. When rarity was defined as either low abundance or small distribution, the greatest number of rare taxa occurred in areas of high taxon richness and naturally fragmented edaphic environments. For both abundance and distributional extent, sexual deception had a significantly higher incidence of rarity than food‐rewarding taxa. There was no significant difference in rarity with site of mycorrhizal infection. Main conclusions While large‐scale edaphic and climatic variation are correlated with orchid taxon turnover and speciation in a similar fashion to the flora in general, the processes responsible for patterns of diversity may differ. Fragmented edaphic environments appear to be associated with a higher incidence of rare species due to limited dispersal/colonization opportunities or radiations of taxa in allopatry. The high incidence of rarity in sexually deceptive taxa could be due to either low fruit set or the risk of specializing on a single pollinator species.     

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.     

LIFE HISTORIES, DENSITY AND BIOMASS IN A WOODLAND SNAIL COMMUNITY

Data, based on 8 monthly sets of random samples, are presentedon the life histories, densities and biomass of snail populationsin a mixed deciduous wood with moderately rich soil. Discus rotundatus, Oxychilus helveticus, O. cellarius and Trichiahispida have approximately annual life cycles, with rather littlepost-reproductive survival. Aegopinella nitiduta and Cochlodinalaminata take two years to reach maturity, and adults of thelatter may survive for several years. Breeding seasons are prolonged,but annual species peak in the autumn. Density does not vary much with season. Mean annual densityof all species combined (37.m^–2) is much lower than thoserecorded for similar woods elsewhere, but the estimate of meanannual standing crop (175 mg ashfree dry weight m^–2) doesnot show the same discrepancy. Comparisons reveal that the maincause of low density is the absence or rarity of several verysmall litter-dwelling species which have little effect on overallbiomass, and reasons for this are discussed. (Received 27 January 1981;     

Predicting mountain plant richness and rarity from space using satellite-derived vegetation indices

Can species richness and rarity be predicted from space? If satellite‐derived vegetation indices can provide us with accurate predictions of richness and rarity in an area, they can serve as an excellent tool in diversity and conservation research, especially in inaccessible areas. The increasing availability of high‐resolution satellite images is enabling us to study this question more carefully. We sampled plant richness and rarity in 34 quadrats (1000 m²) along an elevation gradient between 300 and 2200 m focusing on Mount Hermon as a case study. We then used 10 Landsat, Aster, and QuickBird satellite images ranging over several seasons, going up to very high resolutions, to examine the relationship between plant richness, rarity, and vegetation indices calculated from the images. We used the normalized difference vegetation index (NDVI), one of the most commonly used vegetation indexes, which is strongly correlated to primary production both globally and locally (in more seasonal and in drier and/or colder environments that have wide ranges of NDVI values). All images showed a positive significant correlation between NDVI and both plant species richness and percentage tree cover (with R² as high as 0.87 between NDVI and total plant richness and 0.89 for annual plant richness). The high resolution images enabled us to examine spatial heterogeneity in NDVI within our quadrats. Plant richness was significantly correlated with the standard deviation of NDVI values (but not with their coefficient of variation) within quadrats and between images. Contrary to richness, relative range size rarity was negatively correlated with NDVI in all images, this result being significant in most cases. Thus, given that they are validated by fieldwork, satellite‐derived indices can shed light on richness and even rarity patterns in mountains, many of which are important biodiversity centres.     

Predictive value of biological species for plant conservation in the Mediterranean area]

The validity of Raunkiaer's biological types (or life-forms) was tested on native Corsican flora, using criteria of altitudinal distribution and rarity. The biological basis of this classification has been widely confirmed. The analysis of floras from Corsica and Provence revealed the major role played by both altitude and human impact, and also demonstrated the importance of the predictive value of life-forms to plant conservation. In Southeastern France, there are no clear proportional relationships between rarity and extinction percentages. With increasing levels of human activity, rarity percentages are seen to increase for nearly all types. Conversely, extinction percentages exhibit a clear progression only for the most threatened life-forms: bulb and tuber geophytes, therophytes, parasites and especially hydrophytes. Thus, priority should be given to the protection of these 4 herbaceous types, which are found at low altitudes and lack visible vegetative organs during the unfavourable season.