Lycoperdon perlatum

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Lycoperdon perlatum
Single lycoperdon perlatum.jpg
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Eukaryota
Kingdom: Fungi
Division: Basidiomycota
Class: Agaricomycetes
Order: Agaricales
Family: Agaricaceae
Genus: Lycoperdon
Species:
L. perlatum
Binomial name
Lycoperdon perlatum
Pers. (1796)
Synonyms [1] [2]
  • Lycoperdon gemmatum Batsch (1783)
  • Lycoperdon gemmatum var. perlatum(Pers.) Fr. (1829)
  • Lycoperdon bonordenii Massee (1887)
  • Lycoperdon perlatum var. bonordenii(Massee) Perdeck (1950)
Information icon.svg
Gleba icon.png Glebal hymenium
Convex cap icon.svg Cap is convex
NA cap icon.svg Hymenium attachment is irregular or not applicable
Bare stipe icon.svg Stipe is bare
Transparent spore print icon.svg
 Spore print is brown
Saprotrophic fungus.svgEcology is saprotrophic
Mycomorphbox Choice.pngMycomorphbox Inedible.pngEdibility is choice or inedible

Lycoperdon perlatum, popularly known as the common puffball, warted puffball, gem-studded puffball or devil's snuff-box, is a species of puffball fungus in the family Agaricaceae. A widespread species with a cosmopolitan distribution, it is a medium-sized puffball with a round fruit body tapering to a wide stalk, and dimensions of 1.5 to 6 cm (5⁄8 to 2+3⁄8 in) wide by 3 to 10 cm (1+1⁄8 to 3+7⁄8 in) tall. It is off-white with a top covered in short spiny bumps or "jewels", which are easily rubbed off to leave a netlike pattern on the surface. When mature it becomes brown, and a hole in the top opens to release spores in a burst when the body is compressed by touch or falling raindrops.

Contents

Common puffball, releasing spores in a burst by compressing the body

The puffball grows in fields, gardens, and along roadsides, as well as in grassy clearings in woods. It is edible when young and the internal flesh is completely white, although care must be taken to avoid confusion with immature fruit bodies of poisonous Amanita species. L. perlatum can usually be distinguished from other similar puffballs by differences in surface texture. Several chemical compounds have been isolated and identified from the fruit bodies of L. perlatum, including sterol derivatives, volatile compounds that give the puffball its flavor and odor, and the unusual amino acid lycoperdic acid. Extracts of the puffball have antimicrobial and antifungal activities.

Taxonomy

The species was first described in the scientific literature in 1796 by mycologist Christiaan Hendrik Persoon. [3] Synonyms include Lycoperdon gemmatum (as described by August Batsch in 1783 [4] ); the variety Lycoperdon gemmatum var. perlatum (published by Elias Magnus Fries in 1829 [5] ); Lycoperdon bonordenii (George Edward Massee, 1887 [6] ); and Lycoperdon perlatum var. bonordenii (A.C. Perdeck, 1950 [7] ). [1] [2]

L. perlatum is the type species of the genus Lycoperdon. Molecular analyses suggest a close phylogenetic relationship with L. marginatum . [8]

The specific epithet perlatum is Latin for "widespread". [9] It is commonly known as the common puffball, the gem-studded puffball [10] (or gemmed puffball [11] ), the warted puffball, [9] or the devil's snuff-box; [12] Samuel Frederick Gray called it the pearly puff-ball in his 1821 work A Natural Arrangement of British Plants. [13] Because some indigenous peoples believed that the spores caused blindness, the puffball has some local names such as "blindman's bellows" and "no-eyes". [14]

Description

Lycoperdon perlatum 66070.jpg
The exoperidium is covered in spines and warts.
Lycoperdon perlatum 147481.jpg
Fruit bodies are edible when the gleba is white and firm.

The fruit body ranges in shape from pear-like with a flattened top, to nearly spherical, and reaches dimensions of 1.5 to 6 cm (5⁄8 to 2+3⁄8 in) wide by 3 to 7 cm (1+1⁄8 to 2+3⁄4 in) tall. It has a stem-like base, and is whitish before browning in age. [15] The outer surface of the fruit body (the exoperidium) is covered in short cone-shaped spines that are interspersed with granular warts. The spines, which are whitish, gray, or brown, can be easily rubbed off, and leave reticulate pock marks or scars after they are removed. [11] The base of the puffball is thick. It is initially white, but turns yellow, olive, or brownish in age. [11] The reticulate pattern resulting from the rubbed-off spines is less evident on the base. [16]

In maturity, the exoperidium at the top of the puffball sloughs away, revealing a pre-formed hole (ostiole) in the endoperidium, through which the spores can escape. [17] In young puffballs, the internal contents, the gleba, is white and firm, but turns brown and powdery as the spores mature. [11] The gleba contains minute chambers that are lined with hymenium (the fertile, spore-bearing tissue); the chambers collapse when the spores mature. [17] Mature puffballs release their powdery spores through the ostiole when they are compressed by touch or falling raindrops. A study of the spore release mechanism in L. pyriforme using high-speed schlieren photography determined that raindrops of 1 mm diameter or greater, including rain drips from nearby trees, were sufficient to cause spore discharge. The puffed spores are ejected from the ostiole at a velocity of about 100 cm/second to form a centimeter-tall cloud one-hundredth of a second after impact. A single puff like this can release over a million spores. [18]

Common puffball (Lycoperdon perlatum) Parelstuifzwam (Lycoperdon perlatum).jpg
Common puffball (Lycoperdon perlatum)
Lycoperdon perlatum 64509.jpg
Closeup of the ostiole. Note the pockmarks left behind from missing spines.
Lycoperdon perlatum 74661.jpg
Spores are thick-walled and spherical, measuring roughly 4 μm in diameter.

The spores are spherical, thick-walled, covered with minute spines, and measure 3.5–4.5  μm in diameter. The capillitia (threadlike filaments in the gleba in which spores are embedded) are yellow-brown to brownish in color, lack septae, [19] and measure 3–7.5 μm in diameter. [16] The basidia (spore-bearing cells) are club-shaped, four-spored, and measure 7–9 by 4–5 μm. The basidia bear four slender sterigmata of unequal length ranging from 5–10 μm long. The surface spines are made of chains of pseudoparenchymatous hyphae (resembling the parenchyma of higher plants), in which the individual hyphal cells are spherical to elliptical in shape, thick-walled (up to 1 μm), and measure 13–40 by 9–35 μm. These hyphae do not have clamp connections. [20]

Edibility

Lycoperdon perlatum, dried [21]
Nutritional value per 100 g (3.5 oz)
Energy 1,845.5 kJ (441.1 kcal)
42 g
Fat
10.6 g
44.9 g
Minerals Quantity
%DV†
Copper
25%
0.5 mg
Iron
42%
5.5 mg
Manganese
29%
0.6 mg
Zinc
5%
0.5 mg
†Percentages are roughly approximated using US recommendations for adults.
Source: USDA FoodData Central

Lycoperdon perlatum is considered to be a good edible mushroom when young, when the gleba is still homogeneous and white. [22] They have been referred to as "poor man's sweetbread" due to their texture and flavor. The fruit bodies can be eaten after slicing and frying in batter or egg and breadcrumbs, [12] or used in soups as a substitute for dumplings. [23] As early as 1861, Elias Fries recommended them dried and served with salt, pepper, and oil. [24] The puffballs become inedible as they mature: the gleba becomes yellow-tinged then finally develops into a mass of powdery olive-green spores. L. perlatum is one of several edible species sold in markets in the Mexican states of Puebla and Tlaxcala. [25] [26] The fruit bodies are appealing to animals as well: the northern flying squirrel (Glaucomys sabrinus) includes the puffball in their diet of non-truffle fungi, [27] while the "puffball beetle" Caenocara subglobosum uses the fruit body for shelter and breeding. [28] Nutritional analysis indicates that the puffballs are a good source of protein, carbohydrates, fats, and several micronutrients. [21] The predominant fatty acids in the puffball are linoleic acid (37% of the total fatty acids), oleic acid (24%), palmitic acid (14.5%), and stearic acid (6.4%). [29]

The immature 'buttons' or 'eggs' of deadly Amanita species can be confused with puffballs. This can be avoided by slicing fruit bodies vertically and inspecting them for the internal developing structures of a mushroom, which would indicate the poisonous Amanita. Additionally, amanitas will generally not have "jewels" or a bumpy external surface. [30]

The spores' surfaces have many microscopic spines and can cause severe irritation of the lung (lycoperdonosis) when inhaled. [31] [32] This condition has been reported to afflict dogs that play or run where the puffballs are present. [33] [34]

Similar species

Handkea excipuliformis (Scop.) Kreisel, 1989 (Pestle Puffball) (2) crop.jpg
2011-07-16 Lycoperdon marginatum Vittad 200130.jpg
Lycoperdon excipuliforme (left) and L. marginatum (right) are two of several lookalike puffball species.

There are several other puffball species with which L. perlatum might be confused. L. nettyanum , found in the Pacific Northwest region of the United States, is covered in granular patches, but these granules adhere more strongly to the surface than those of L. perlatum. [35] L. pyriforme lacks prominent spines on the surface, and grows on rotting wood—although if growing on buried wood, it may appear to be terrestrial. The widely distributed and common L. umbrinum has spines that do not leave scars when rubbed off, [36] a gleba that varies in color from dark brown to purple-brown at maturity, and a purple-tinged base. The small and rare species L. muscorum grows in deep moss. L. peckii can be distinguished from L. pyriforme by the lavender-tinged spines it has when young. L. rimulatum has purplish spores, and an almost completely smooth exoperidium. [11] L. excipuliforme is larger and grayer, and, in mature individuals, the upper portion of its fruit body breaks down completely to release its spores. [14] In the field, L. marginatum is distinguished from L. perlatum by the way in which the spines are shed from the exoperidium in irregular sheets. [36]

Ecology and distribution

Fruit bodies may grow singly, scattered, in groups, or--as shown here--in clusters. Lycoperdon perlatum 95340.jpg
Fruit bodies may grow singly, scattered, in groups, or—as shown here—in clusters.

A saprobic species, Lycoperdon perlatum grows solitarily, scattered, or in groups or clusters on the ground. It can also grow in fairy rings. [12] Typical habitats include woods, grassy areas, and along roads. [11] It has been reported from Pinus patula plantations in Tamil Nadu, India. [20] The puffball sometimes confuses golfers because of its resemblance to a golf ball when viewed from a distance. [12]

A widespread species with an almost cosmopolitan distribution, [16] it has been reported from Africa (Kenya, Rwanda, [37] Tanzania [38] ), Asia (China, [39] Himalayas, [40] Japan, [41] southern India [20] Iran [42] ), Australia, [12] Europe, [43] New Zealand, [44] and South America (Brazil). [45] It has been collected from subarctic areas of Greenland, and subalpine regions in Iceland. [46] In North America, where it is considered the most common puffball species, it ranges from Alaska [47] to Mexico, [48] although it is less common in Central America. [49] The species is popular on postage stamps, and has been depicted on stamps from Guinea, Paraguay, Romania, Sierra Leone, and Sweden. [50]

The puffball bioaccumulates heavy metals present in the soil, [51] [52] and can be used as a bioindicator of soil pollution by heavy metals and selenium. [53] In one 1977 study, samples collected from grassy areas near the side of an interstate highway in Connecticut were shown to have high concentrations of cadmium and lead. [54] L. perlatum biomass has been shown experimentally to remove mercury ions from aqueous solutions, and is being investigated for potential use as a low-cost, renewable, biosorptive material in the treatment of water and wastewater containing mercury. [55]

Chemistry

Lycoperdic acid is an amino acid known only from L. perlatum. Lycoperdic acid.png
Lycoperdic acid is an amino acid known only from L. perlatum.

Several steroid derivatives have been isolated and identified from fruit bodies of L. perlatum, including (S)-23-hydroxylanostrol, ergosterol α-endoperoxide, ergosterol 9,11-dehydroendoperoxide and (23E)-lanosta-8,23-dien-3β,25-diol. The compounds 3-octanone, 1-octen-3-ol, and (Z)-3-octen-1-ol are the predominant components of the volatile chemicals that give the puffball its odor and flavor. [56] Extracts of the puffball contain relatively high levels of antimicrobial activity against laboratory cultures of the human pathogenic bacteria Bacillus subtilis , Staphylococcus aureus , Escherichia coli , and Pseudomonas aeruginosa , with activity comparable to that of the antibiotic ampicillin. [57] These results corroborate an earlier study that additionally reported antibacterial activity against Salmonella enterica serovar Typhimurium, Streptococcus pyogenes , and Mycobacterium smegmatis . [58] Extracts of the puffball have also been reported to have antifungal activity against Candida albicans , C. tropicalis , Aspergillus fumigatus , Alternaria solani , Botrytis cinerea , and Verticillium dahliae . [59] A 2009 study found L. perlatum puffballs to contain cinnamic acid at a concentration of about 14 milligrams per kilogram of mushroom. [60] The fruit bodies contain the pigment melanin. [61]

The amino acid lycoperdic acid (chemical name 3-(5(S)-carboxy-2-oxotetrahydrofuran-5(S)-yl)-2(S)-alanine) was isolated from the puffball, and reported in a 1978 publication. [62] Based on the structural similarity of the new amino acid with (S)-glutamic acid, (S)-(+)-lycoperdic acid is expected to have antagonistic or agonistic activity for the glutamate receptor in the mammalian central nervous system. Methods to synthesize the compounds were reported in 1992, [63] 1995, [64] and 2002. [65]

Related Research Articles

<span class="mw-page-title-main">Puffball</span> Fungus

Puffballs are a type of fungus featuring a ball-shaped fruit body that bursts on contact or impact, releasing a cloud of dust-like spores into the surrounding area. Puffballs belong to the division Basidiomycota and encompass several genera, including Calvatia, Calbovista and Lycoperdon. The puffballs were previously treated as a taxonomic group called the Gasteromycetes or Gasteromycetidae, but they are now known to be a polyphyletic assemblage.

<i>Calvatia gigantea</i> Species of mushroom

Calvatia gigantea, commonly known in English as the giant puffball, is a puffball mushroom commonly found in meadows, fields, and deciduous forests in late summer and autumn. It is found in temperate areas throughout the world.

<i>Lycoperdon umbrinum</i> Umber-brown puffball, a fungus

Lycoperdon umbrinum, commonly known as the umber-brown puffball, is a type of Puffball mushroom in the genus Lycoperdon. It is found in China, Europe, Africa, and North America.

<i>Calvatia craniiformis</i> Species of puffball fungus

Calvatia craniiformis, commonly known as the brain puffball or the skull-shaped puffball, is a species of puffball fungus in the family Agaricaceae. It is found in Asia, Australia, and North America, where it grows on the ground in open woods. Its name, derived from the same Latin root as cranium, alludes to its resemblance to an animal's brain. The skull-shaped fruit body is 8–20 cm (3–8 in) broad by 6–20 cm (2–8 in) tall and white to tan. Initially smooth, the skin (peridium) develops wrinkles and folds as it matures, cracking and flaking with age. The peridium eventually sloughs away, exposing a powdery yellow-brown to greenish-yellow spore mass. The puffball is edible when the gleba is still white and firm, before it matures to become yellow-brown and powdery. Mature specimens have been used in the traditional or folk medicines of China, Japan, and the Ojibwe as a hemostatic or wound dressing agent. Several bioactive compounds have been isolated and identified from the brain puffball.

<i>Apioperdon</i> Genus of fungi

Apioperdon pyriforme commonly known as the pear-shaped puffball or stump puffball, is a saprobic fungus present throughout much of the world. Emerging in autumn, this puffball is common and abundant on decaying logs of both deciduous and coniferous wood. It is considered a choice edible when still immature and the inner flesh is white. It is often called Lycoperdon pyriforme, but was transferred to Apioperdon in 2017 based on phylogenetic and morphological differences. It is the only species in the genus.

<i>Bovista</i> Genus of fungi

Bovista is a genus of fungi commonly known as the true puffballs. It was formerly classified within the now-obsolete order Lycoperdales, which, following a restructuring of fungal taxonomy brought about by molecular phylogeny, has been split; the species of Bovista are now placed in the family Agaricaceae of the order Agaricales. Bovista species have a collectively widespread distribution, and are found largely in temperate regions of the world. Various species have historically been used in homeopathic preparations.

<i>Bovista plumbea</i> Species of fungus

Bovista plumbea, also referred to as the paltry puffball, is a small puffball mushroom commonly found in Western Europe and California, white when young and greyish in age. Easily confused with immature Bovista dermoxantha, it is attached to the substrate by a tuft of mycelium.

<i>Bovista nigrescens</i> Species of fungus

Bovista nigrescens, commonly referred to as the brown puffball or black bovist, is an edible cream white or brown puffball. Phylogenetic relationships between Bovista nigrescens and species of Lycoperdaceae were established based on ITS and LSU sequence data from north European taxa.

<i>Handkea utriformis</i> Species of fungus

Handkea utriformis, synonymous with Lycoperdon utriforme, Lycoperdon caelatum or Calvatia utriformis, is a species of the puffball family Lycoperdaceae. A rather large mushroom, it may reach dimensions of up to 25 cm (10 in) broad by 20 cm (8 in) tall. It is commonly known as the mosaic puffball, a reference to the polygonal-shaped segments the outer surface of the fruiting body develops as it matures. Widespread in northern temperate zones, it is found frequently on pastures and sandy heaths, and is edible when young. H. utriformis has antibiotic activity against a number of bacteria, and can bioaccumulate the trace metals copper and zinc to relatively high concentrations.

<i>Astraeus hygrometricus</i> Cosmopolitan species of fungus in the family Diplocystaceae.

Astraeus hygrometricus, commonly known as the hygroscopic earthstar, the barometer earthstar, or the false earthstar, is a species of fungus in the family Diplocystaceae. Young specimens resemble a puffball when unopened. In maturity, the mushroom displays the characteristic earthstar shape that is a result of the outer layer of fruit body tissue splitting open in a star-like manner. The false earthstar is an ectomycorrhizal species that grows in association with various trees, especially in sandy soils. A. hygrometricus was previously thought to have a cosmopolitan distribution, though it is now thought to be restricted to Southern Europe, and Astraeus are common in temperate and tropical regions. Its common names refer to the fact that it is hygroscopic (water-absorbing) and can open up its rays to expose the spore sac in response to increased humidity, then close them up again in drier conditions. The rays have an irregularly cracked surface, while the spore case is pale brown and smooth with an irregular slit or tear at the top. The gleba is white initially, but turns brown and powdery when the spores mature. The spores are reddish-brown and roughly spherical with minute warts, measuring 7.5–11 micrometers in diameter.

<i>Bovista aestivalis</i> Species of fungus

Bovista aestivalis is a species of small puffball in the family Agaricaceae. It is generally found in the coastal regions of California, but was reported from Korea in 2015. This fungus is often confused with Bovista dermoxantha, because of its similar peridium, and Bovista plumbea. The surest way to tell the species apart is to examine the spores and exoperidium, respectively, with a microscope.

<i>Geastrum triplex</i> Species of fungus in the family Geastraceae

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<i>Calvatia sculpta</i> Species of puffball fungus in the family Agaricaceae

Calvatia sculpta, commonly known as the sculpted puffball, the sculptured puffball, the pyramid puffball, and the Sierran puffball, is a species of puffball fungus in the family Agaricaceae. Attaining dimensions of up to 8 to 15 cm tall by 8 to 10 cm wide, the pear- or egg-shaped puffball is readily recognizable because of the large pyramidal or polygonal warts covering its surface. It is edible when young, before the spores inside the fruit body disintegrate into a brownish powder. The spores are roughly spherical, and have wart-like projections on their surfaces.

<i>Calbovista</i> Genus of fungi

Calbovista is a fungal genus containing the single species Calbovista subsculpta, commonly known as the sculptured puffball, sculptured giant puffball, and warted giant puffball. It is a common puffball of the Rocky Mountains and Pacific Coast ranges of western North America. The puffball is more or less round with a diameter of up to 15 cm (6 in), white becoming brownish in age, and covered with shallow pyramid-shaped plates or scales. It fruits singly or in groups along roads and in open woods at high elevations, from summer to autumn.

<i>Mycenastrum</i> Genus of fungi

Mycenastrum is a fungal genus in the family Agaricaceae. The genus is monotypic, containing one widely distributed species, Mycenastrum corium, known by various common names: the giant pasture puffball, leathery puffball, or tough puffball. The roughly spherical to turnip-shaped puffball-like fruit bodies grow to a diameter of 6–24 cm (2–9 in). Initially covered by a thick, felted, whitish layer, the puffballs develop a characteristic checkered skin (peridium) in age. When the internal spore mass, the gleba, is firm and white, the puffball is edible, although some individuals may suffer mild gastrointestinal symptoms after eating it. As the spores mature, the gleba turns first yellowish then purplish brown. Spores are released when the peridium eventually splits open into irregularly shaped sections. Microscopically, the gleba consists of spherical, dark brown spores with rounded bumps on their surfaces, and a capillitium—intricately branched fibers that form long thorn-like spines. The puffball grows on or in the ground in prairie or desert habitats. Although widely distributed, it is not commonly encountered. Mycenastrum corium is a threatened species in Europe.

<i>Lycoperdon echinatum</i> Species of puffball mushroom

Lycoperdon echinatum, commonly known as the spiny puffball or the spring puffball, is a type of puffball mushroom in the family Agaricaceae. The saprobic species has been found in Africa, Europe, Central America, and North America, where it grows on soil in deciduous woods, glades, and pastures. It has been proposed that North American specimens be considered a separate species, Lycoperdon americanum, but this suggestion has not been followed by most authors. Molecular analysis indicates that L. echinatum is closely related to the puffball genus Handkea.

<i>Handkea excipuliformis</i> Species of fungus

Handkea excipuliformis, commonly known as the pestle puffball or long-stemmed puffball, is a species of the family Agaricaceae. A rather large puffball, it may reach dimensions of up to 15 cm (5.9 in) broad by 25 cm (9.8 in) tall. Widespread in northern temperate zones, it is found frequently on pastures and sandy heaths.

<i>Lycoperdon marginatum</i> Species of fungus

Lycoperdon marginatum, commonly known as the peeling puffball, is a type of puffball mushroom in the genus Lycoperdon. A common species, it is found in Europe and North America, where it grows on the ground. It is characterized by the way that the spiny outer layer peels off in sheets.

<i>Scleroderma polyrhizum</i> Species of fungus

Scleroderma polyrhizum, commonly known as the star earthball or dead man's hand, is a basidiomycete fungus and a member of the genus Scleroderma, or "earthballs". Found in dry, sandy soils, this species begins completely buried before slowly forcing the soil aside as it cracks apart to form a rough, star-shaped body with a diameter of 12–15 cm (4.7–5.9 in). At the center is the dark, brownish spore mass. Widely distributed wherever the soil and climate are favorable, it is known from Asia, Europe, and the Americas.

<i>Bovista pila</i> Species of fungus

Bovista pila, commonly known as the tumbling puffball, is a species of puffball fungus in the family Agaricaceae. A temperate species, it is widely distributed in North America, where it grows on the ground on road sides, in pastures, grassy areas, and open woods. There are few well-documented occurrences of B. pila outside North America. B. pila closely resembles the European B. nigrescens, from which it can be reliably distinguished only by microscopic characteristics.

References

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  14. 1 2 Roberts P, Evans S (2011). The Book of Fungi. Chicago, Illinois: University of Chicago Press. p. 520. ISBN   978-0-226-72117-0.
  15. ↑ Trudell, Steve; Ammirati, Joe (2009). Mushrooms of the Pacific Northwest. Timber Press Field Guides. Portland, OR: Timber Press. pp. 269–270. ISBN   978-0-88192-935-5.
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  17. 1 2 Miller HR, Miller OK (1988). Gasteromycetes: Morphological and Developmental Features, with Keys to the Orders, Families, and Genera. Eureka, California: Mad River Press. p. 40. ISBN   0-916422-74-7.
  18. ↑ Gregory PH (1949). "The operation of the puff-ball mechanism of Lycoperdon perlatum by raindrops shown by ultra-high-speed Schlieren cinematography". Transactions of the British Mycological Society. 32 (1): 11–5. doi:10.1016/S0007-1536(49)80030-1.
  19. ↑ Miller HR, Miller OK (2006). North American Mushrooms: A Field Guide to Edible and Inedible Fungi. Guilford, Connecticut: Falcon Guide. p. 453. ISBN   0-7627-3109-5.
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  21. 1 2 Nutritional values are based on chemical analysis of Turkish specimens, conducted by Colak and colleagues at the Department of Chemistry, Karadeniz Technical University. Source: Colak A, Faiz Ö, Sesli E (2009). "Nutritional composition of some wild edible mushrooms" (PDF). Türk Biyokimya Dergisi [Turkish Journal of Biochemistry]. 34 (1): 25–31. Archived from the original (PDF) on 17 July 2011. Retrieved 14 September 2011.
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