Bioaccumulation of Heavy Metals in Common Carp: Implications for Human Health

Abstract

Zn, Ni, Cr, Cu, Cd and Pb were examined in the muscle, intestine, liver, skin and gills of common carp, Cyprinus carpio. Aim of the study was to quantify the accumulation of these metals in various organs and to determine whether these levels pose a human health concern. Our finding fix the metal bioaccumulation order in the muscle of Cyprinus carpio was Zn>Cr>Cu>Pb>Ni>Cd, in the intestine was Zn>Pb>Cr>Cu>Ni>Cd, in the liver was Zn>Cr>Cr>Pb>Ni>Cd, in the skin was Zn>Cr>Pb>Cu>Ni>Cd and in the gills was Zn>Cr>Cu>Pb>Ni>Cd. Overall heavy metals burden was in the order of Zn>Cr>Pb>Cu>Ni>Cd. Different tissues of the fish accumulated heavy metals in the order of intestine>skin>liver>gills>muscle. Intestine being the prime target organ indicates the route of the metal uptake was the direct result of dietary exposure. Although muscle accumulated the least level of metals but even then Pb, Ni and Cd in muscle exceed the US, RDA limits and pose a health concern for fish consumers.

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NTERNATIONAL
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GRICULTURE
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IOLOGY
ISSN Print: 1560–8530; ISSN Online: 1814–9596
13–393/2014/16–3–571–577
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Full Length Article
To cite this paper:
Yousaf,
N.,
M. Fiaz, H. Ahmad and
A.N. Khalid. 2014, Gasteroid mycota of district Mansehra, Khyber Pakhtunkhwa, Pakistan. Int. J.
Agric. Biol., 16: 571‒577
Gasteroid Mycota of District Mansehra, Khyber Pakhtunkhwa, Pakistan
Nousheen
Yousaf
1*
,
Muhammad Fiaz
2
, Habib Ahmad
3
and
Abdul Nasir Khalid
1
1
Department of Botany, University of the Punjab, Lahore, 54590, Pakistan
2
Department of Botany Hazara University, Mansehra, KPK, Pakistan
3
Department of Genetics Hazara University, Mansehra, KPK, Pakistan
*For correspondence:
nousheenyousaf@gmail.com
Abstract
During the exploration of basidiomycetes of Pakistan, twenty gasteroid fungi were collected and identified from district
Mansehra, Pakistan. Out of these, nine specimens represented different taxa; two belong to genera Geastrum and Lycoperdon,
one each species belonged to genera Astraeus, Bovista, Phallus, Pisolithus, and Scleroderma. These gasteroid taxa have been
identified, described and discussed. Among these, Phallus hadriani is a second report for Pakistan, and four gasteroid taxa are
new records for District Mansehra. © 2014 Friends Science Publishers
Keywords:
Basidiomycota; Diversity; Gasteromycetes; Taxonomy
Introduction
District Mansehra is located in Hazara civil division of the
Khyber Pakhtunkhwa Province, Pakistan. It is situated
between 34
o
–14’ and 35
o
–11’ north latitudes and 72
o
–49’
and 74
o
–08’ east longitude. It consists of Mansehra, Balakot
and Oghi tehsils. The district spread over an area of 5959
km
2
(Shah and Khan, 2006) and has been blessed with high
mountains, lakes, beautiful valleys, plains and more
especially the rich and harmonious combination of tall and
stately fine trees. The mountains of the northern side are
also the extension of the same mountain system. From the
north east, Musa-ka-Musala a peak (4080 meters), which
lies along the north eastern side of Konsh and Bhogarmang
valleys (Mustafa, 2003). On the western side of Agror
valley (Oghi) there is a famous black mountain range which
runs northwards (Mustafa, 2003). The climate of the district
is moist temperate with seasonal periods of rainfall, snow,
and drought (Mustafa, 2003). Forests of the district are rich
in trees as Deodar, Blue pine, Chirr, Walnut, Cherry, Poplar
and Kao (SMEDA, 2009) and supports a rich diversity of
macro fungi during monsoon. Gasteroid fungi represent a
major group belonging to macro fungi. Most of the
members of this group viz., Astraeus, Pisolithus,
Scleroderma are involved in ectomycorrhizal associations
with some coniferous trees (Martin, 2001; Turjaman et al.,
2005; Pyasi et al., 2011; Kaewgrajang et al., 2013). Some
members belonging to genus Bovista, Lycoperdon are edible
and have medicinal value (Lans et al., 2007, Ramesh and
Pattar, 2010).
So far only 17 gasteroid fungi have been reported from
different areas of district Mansehra (Ahmad, 1939, 1952a, b,
1956, 1969, Khan 1968, Ahmad et al., 1997). In present
investigation, nine gasteroid taxa have been reported, out of
which one is new record for the country, four are new
record for district Mansehra and 5 taxa are being described
from different localities of district Mansehra for the first
time.
Materials and Methods
Basidiomata were collected with the help of a sharp digger
avoiding the loss of rhizomorphs. Specimens were dried
manually and brought to laboratory for further investigation.
Morphological characters (e.g., basidiospores, capillitium,
endoperidium, and exoperidium) were observed
macroscopically using a stereomicroscope (Meiji Techno
EMZ-5TR) and studied under light microscope (Nikon YS
100) at high magnification (1600x). Glebal material was
examined when mounted in lacto-phenol and 5% KOH
medium. Illustrations of microscopic features were prepared
with the help of a camera Lucida (Ernst Leitz Wetzlar
Germany) fitted to a light microscope.
Specimens were identified with the help of literature
(Coker and Couch 1928; Bottomly, 1948; Miller and Miller,
1988; Ellis and Ellis, 1990; Pegler and Spooner 1995). All
of the specimens have been deposited in the collection of
gasteroid fungi at the LAH Herbarium, Department of
Botany, University of the Punjab, Lahore, Pakistan.
Results
Taxonomy
Astraeus hygrometricus (Pers.) Morgan, J. Cincinnati Soc.
Nat. Hist. 12: 20 (1889) (Fig. 1A–B, 4).

Yousaf et al. / Int. J. Agric. Biol., Vol. 16, No. 3, 2014
572
Mature gasterocarps globose to depressed globose,
sessile, 25–50 mm in diam. when mature, splitting in a
stellate pattern, encrusted with soil particles and other
debris material, odour not recorded. Peridium double.
Exoperidium up to 1.5 mm thick, splitting in to 5-9 acute
rays; rays expanded when fresh, recurved inward upon
drying; composed of three layers; mycelial layer, thin,
brown, not persistent; middle layer off-white to grey,
thicker than mycelial layer; inner layer off-white to grey
to brown with age, as thick as middle layer, extensively
cracked in mature specimens. Endoperidium sessile, off-
white to grey, opens by a pore; pore small to medium, up
to 3 mm in diam. Gleba light brown to brown, cottony.
Basidiospores dark brown, ornamented, densely
verrucose, up to 7–11 µm in diam. including ornaments,
(6–11 µm in diam. ornamentation excluded), verrucae up
to 1–1.7 µm long. Capillitium hyaline, thick walled, with
narrow lumen, branched, rarely septate, up to 5.0–12.8
µm in diam., (walls up to 1.9–4.5 µm), clamp connections
present.
Material Examined
Pakistan: Khyber Pakhtunkhwa, District Mansehra, Khabbal
Paien, at 1910 m a.s.l., in groups, among grass, 1
st
Aug.
2010, M. Fiaz, 62 (LAH100100); Dadar, at 1235 m a.s.l.,
solitary, 1
st
Aug. 2010, M. Fiaz, FM226, (HUP Herbarium
No. MFG–321), (LAH100101).
Comments
Astra eus hygrometricus was reported first time by Ahmad
in 1956 as Geastrum hygrometricum, from different regions
of Pakistan viz., Patriata (Murree) of Punjab, Kalam (Swat),
Kaghan Valley of KPK. It is reported first time from
Khabbal Paien, and Dadar of district Mansehra.
Bovista plumbea Pers., Ann. Bot. (Usteri) 15: 4 (1795) (Fig.
1C and Fig. 5).
Basidioma 30 mm broad x 25 mm high, globose to
subglobose, off-white when young, solitary, sometimes
gregarious; attached to the substratum via thick tuft of
mycelium; rhizomorphs black, sometimes white, heavily
encrusted with soil particles, dehiscence by an apical pore;
pore small to medium, up to 4 mm in diameter, develops as
exoperidium sloughs off. Exoperidium white when young,
grayish off white when mature, thick, persistent when
young, peeling off upon maturity, in the form of sheets,
firstly from apical portion then below, sometimes patches
can be found all over the gasterocarp, can be seen attached
to the basal part in mature specimens in the form of
weathered, thin membranous layer. Endoperidium mouse
gray when exposed, smooth to rough, papery, sometimes
covered with dust, encrusted with sand particles. Gleba
grayish black, cottony to powdery, pulverulent. Sterile base
absent. Basidiospores sub-globose to oval, dark brown, 3.5–
6 × 4.5–7.5 µm, with central oil droplet, pedicellate, pedicel
Fig. 1: A-D: A. Astraeus hygrometricus, young
basidiomata. B. A. hygrometricus, a mature basidioma. C.
Bovista plumbea, a mature basidioma with exposed
endoperidium. D. Geastrum saccatum. Scale Bar: A = 1.5
cm, B = 0.7 cm, C = 0.5 cm, D = 0.8 cm.
Fig. 2: A–C: A. Geastrum triplex. B. Lycoperdon perlatum
(Gem stud Puff ball). C. Lycoperdon excipuliforme. Scale
Bar: A = 1.2 cm, B = 1.8 cm, C = 1cm.
Fig. 3: A–C: A. Pisolithus tinctorious. B. Phallus
hadriani. C. Scleroderma Bovista. Scale Bar: A and B =
1.5 cm, C = 1 cm

Gasteroid fungi of district Mansehra / Int. J. Agric. Biol., Vol. 16, No. 3, 2014
573
up to 12 µm long, brown to hyaline, tapering, straight to
slightly curved. Capillitium brown, prominent, well
developed, in the form of isolated units, not much
interwoven, thick main axis, with branches originating from
the axis, branches tapers at the ends, aseptate, pores absent,
main axis up to 17 µm thick, branches up to 1.8–4.7 µm
thick, wall thickness from 1.8–5.7 µm.
Material Examined
Pakistan: Khyber Pakhtunkhwa, District Mansehra, Musa-
ka-Musala, at 4062 m a.s.l., solitary, among grass, Aug.
2011, M. Fiaz, M3, (HUP Herbarium No. MFG–323.),
(LAH100102).
Comments
Bovista plumbea is the type species of genus Bovista. It is
characterized by globose fruiting bodies with white
exoperidium and lead grey endoperidium, oval, long
pedicellate basidiospores. It is usually found growing on
grounds and among grasses. It is commonly occurring
gasteroid taxon, reported from different localities of
Pakistan. It has previously been reported from Changla gali,
Bata Kundi (Kaghan Valley), and Kalam (Swat) of KPK by
Ahmad (1952b and 1956). It is being reported from Musa ka
Masala of district Mansehra for first time. It occurs solitary,
sometimes gregarious on ground, among grasses in
Himalayan Moist Temperate Forests of Punjab, Khyber
Fig. 4: A–C: Astraeus hygrometricus.
A. Verrucose basidiospores. B.
Eucapillitial threads. C. Joint like septa
in capillitial threads. Scale Bar: A =
3.5 µm, B = 13 µm, C = 8.5 µm.
Fig. 5. A–D: Bovista plumbea. A.
Pedicellate basidiospores. B.
Eucapillitial thread, thick walled main
axis. C. Eucapillitium, an isolated unit.
D. Endoperidial hyphae. Scale Bar: A
= 6 µm, B = 19.5 µm, C = 48 µm, D =
21 µm.
Fig. 6. A–E: Geastrum saccatum A.
LM imag of capillitial threads. B. LM
image of endoperdial hyphae. C.
Verrucose basidiospores. D. Capillitial
threads. E. Endoperidial hyphae. Scale
Bar: A = 21 µm, B = 26 µm, C = 1.8
µm, D = 16 µm, E = 13 µm.
Fig. 7. A–C: Geastrum triplex. A.
Endoperidial hyphae. B. Verrucose
basidiospores. C. Eucapillitial threads;
thick walled hyphae. Scale Bar. A = 7
µm, B = 5 µm, C = 7.5 µm
Fig. 8. A–E: Lycoperdon perlatum.
A. Exoperidial elements. B. Verrucose
basidiospores. C. Ecapillitium;
aseptate hyphae. D. Endoperidial
hyphae. E. Paracapillitial hyphae.
Scale Bar. A = 13 µm, B = 3 µm, C =
18 µm, D and E = 4 µm.
Fig. 9. A–D: Pisolithus tinctorious. A.
Verruculose basidiospores. B.
Exoperidial hyphae. C. Endoperidial
hyphae. D. Pseudo-peridiole hyphae.
Scale Bar: A = 3 µm, B and C = 13
µm, D = 7 µm.

Yousaf et al. / Int. J. Agric. Biol., Vol. 16, No. 3, 2014
574
Pakhtunkhwa and in alpine vegetation of Gilgit-Batistan.
However, this is first report of its occurrence in drier parts
of the country.
Geastrum saccatum Fr., Syst. mycol. (Lundae) 3(1): 16
(1829) (Fig. 1D and Fig. 6).
Basidioma scattered on soil, at first hypogeous and
ovate, attached with a basal mycelium to the substratum,
expanded on maturity and superficial, up to 4 cm across,
Exoperidium splitting from middle to the tip into 10 non
hygroscopic rays, with acute apices, up to 2 cm in length,
bending downward, upper surface pinkish tan to pale
yellowish to camel brown, occasionally cracking.
Endoperodial body sessile, 2 cm across, globose to
subglobose or slightly depressed, onion shaped when not
depressed, smooth, seated in saccate, slightly depressed
basel area of exoperidium, grayish brown with occasional
darker tints; Peristome fibrillose and conical, dark brown,
surrounded by circular shallow groove. Gleba dull brown,
pulverulent. Basidiospores globose, 3.3–5.2 µm in dia, dark
brown, finely verrucose. Capillitial threads 2–7 µm thick,
coiled, mostly smooth walled, slightly covered by debris,
yellowish to pale brown to brown in KOH. Endoperidial
hyphae densely interwoven, 2–6 µm wide, thick walled,
smooth, sometime undulating and yellowish brown.
Material Examined
Pakistan: Khyber Pakhtunkhwa, District Mansehra, Balakot,
Nadibunglaw, solitary on sandy soil among mix forest of
Abies pindrow Royle, Picea smithiana (Wall.) Boiss and
Pinus wallichiana A. B. Jackson, at 2512 m. a. s. l., 1
st
Aug.
2010. MF # FM–243. (HUP Herbarium No. MFG–326).
Comments
Previously, Geastrum saccatum has only been reported
from Kaghan valley by Ahmad in 1952 and 1956. This is
the seond report of this species from Pakistan. It is a new
record
for
Balakot
and
Nadibunglaw of district
Mansehra.
Geastrum triplex Jungh. [as 'Geaster'], Tijdschr. Nat.
Gesch. Physiol. 7: 287 (1840) (Fig. 2A and Fig. 7).
Basidiomata in groups on soil, expanded fruit body
epigeous, 3–7 cm in dia, attached by a basal mycelial tuft
with substrata. Exoperidium splitting from middle into 5–7
non-hygroscopic, thick and more or less triangular arms,
with cracks and fissures on the upper surface in mature
specimen, often splitting to form collar or saucer shaped
platform having the spore sac seated in it, often the rays turn
downward, uplifting and exposing the spore sac.
Endoperidium sessile, 1.5–3 cm across, globose to onion
shaped, depressed in aged specimen, dull brown or snuff
brown, smooth. Peristome fibrillose, conical, surrounded by
a paler, occasionally depressed circular area. Gleba dull
brown, powdery, collumella distinct. Basidiospores globose
to subglobose, 3.8–5.8 µm in dia, pale brown to dark brown,
finely verrucose. Capillitial threads 2.8–8.5 µm thick,
hyaline to pale yellowish to pale reddish brown, with
gradually tapering or obtuse tips, encrusted. Endoperidial
hyphae compactly arranged, 3–6.6 µm thick, thick walled,
smooth, yellowish.
Material Examined
Pakistan: Khyber Pakhtunkhwa, District Mansehra, Balakot,
Nadibunglaw, Gregarious on soil among mix forest of Abies
pindrow Royle, Picea smithiana (Wall.) Boiss and Pinus
wallichiana A. B. Jackson, at 2512 m. a. s. l., 1
st
Aug. 2010.
MF # FM–222. (HUP Herbarium No. MFG–327a.); Solitary
on ground, Balakot, Nadibunglaw, at 2518 m. a. s. l.,
August 2010. MF # FM–245. (HUP Herbarium No. MFG–
327b).
Comments
It has previously been reported from Kalam (Swat), Shogran
(Kaghan valley), Nathia Gali, Patriata (Murree hills) by
Ahmad in 1952 and 1956, also by Khan in 1968. It is first
time reported from Balakot and Nadibunglaw of district
Mansehra.
Lycoperdon excipuliforme (Scop.) Pers., Syn. meth. fung.
(Göttingen) 1: 143 (1801) (Fig. 2C).
Detailed descriptions and illustrations of Lycoperdon
excipuliforme are available by Yousaf et al. (2012).
Material Examined
Pakistan: Khyber Pakhtunkhwa, District Mansehra, Musa
Ka Musala, at 3894 m a.s.l., in groups, 1
st
Aug. 2010, M.
Fiaz, 245, FM222, (HUP Herbarium No. MFG–328)
(LAH100103).
Comments
It has been reported by Yousaf et al. in 2012 from Nathia
Gali, Khyber Pakhtunkhwa, Pakistan. It is a new record
from district Mansehra.
Fig. 10: A–D. Scleroderma bovista. A. Verrucose
basidiospores. B. Exoperidial hyphae. C. Endoperidial
hyphae. D. Tramal hyphae. Scale Bar: A = 5.5 µm, B and
C = 9.7 µm, D = 18.5 µm

Gasteroid fungi of district Mansehra / Int. J. Agric. Biol., Vol. 16, No. 3, 2014
575
Lycoperdon perlatum Pers., Observ. mycol. (Lipsiae) 1:
145 (1796) (Fig. 2B and Fig. 8).
Basidiomata gregarious, pyriforme, 30–50 mm high
× 15–35 mm broad, off-white when young, brown when
mature; rhizomorphs white encrusted with particles of soil
and other debris material. Dehiscence by an apical pore,
up to 5 mm in diam. Exoperidium consisting of 1 mm
long warts; warts off white, more prominent over spore
case, less evident below, rubbed off when mature,
sometimes adherent in mature specimens. Endoperidium
papery, yellowish brown. Gleba cottony, white when
young, brown later on, up to 1 mm high, comprising 1/3
rd
of gasterocarps. Pseudocolumella present, well
developed. Sterile base comprising of 2/3
rd
of
gasterocarps, chambered, showing two zones of different
colors, upper zone yellowish brown just below the gleba,
lower zone brown to olive. Basidiospores brown, globose
to subglobose, nearly smooth, 3–5 µm in diam.,
pedicellate; pedicel up to 1.2 µm, hyaline. Eucapillitium
brown, Lycoperdon type, well developed, aseptate,
frequently branched, pores absent, up to 2–7 µm in diam.,
wall thickness up to 1.6 µ m, branches with tapering ends,
straight to sub undulate, often bulging at some points.
Paracapillitium present, hyaline, septate, branched, joint
like septa also present, up to 5 µm in diam. Exoperidium
composed of hyaline, globose to subglobose to elongated
hyphal elements, up to 30 µm high, 9.5 µm broad.
Endoperidium composed of thin walled, aseptate, tightly
packed hyphal elements, up to 5 µm in diam.
Material Examined
PAKISTAN: K
HYBER
P
AKHTUN
K
HWA
, District
Mansehra, Khabbal Paien, Ucharhi, at 1825 m a.s.l., in
groups, 1
st
Aug. 2010, M. Fiaz, F-04, (HUP Herbarium
No. MFG–329). (LAH100104).
Comments
It is the most commonly occurring Lycoperdon sp. in moist
temperate region of Pakistan. It has been reported from
Patriata (Murree), Changla gali, Bahrain (Swat), Shogran,
Sharan (Kaghan Valley) by Ahmad in 1952 and 1956. It is
first report of this taxon from Khabbal Paein and Ucharhi of
district Mansehra.
Phallus hadriani Vent., Mém. Inst. nat. Sci. Arts 1: 517
(1798) (Fig. 3B).
Mature basidioma gray with violet tone, up to 125
mm high, attached to the substratum by well-developed
mycelial base; Rhizomorphs off white. Receptaculum
with off white reticulate pileus head and stipe; Pileus up
to 30 mm in height × 25 mm in diam., campanulate,
hollow. Gleba olivaceous green wet, sticky, deliquescent.
Stipe hollow, off white, spongy, up to 80 mm in height ×
17-20 mm in diam., cylindrical. Volva globose, thick, soft,
cup shaped, covering 1/3
rd
of the stipe, grayish to violet,
lined with grayish to violet gelatinous and sticky material
inside, up to 37 mm in height × 35 mm in diam.
Material Examined
Pakistan, Khyber Pakhtunkhwa, District Mansehra, Chattar
Plain near PTDC hotel, at 1320 m a. s. l., September 2011.
MF # FM–P1. (HUP Herbarium No. MFG–330). Bt-8,
(LAH100105).
Comments
Phallus hadriani is a new record for District Mansehra. It
is the second report of this species from Pakistan
.
Pisolithus tinctorius (Mont.) E. Fisch., (1900) (Fig. 3A and
Fig. 9).
Detailed descriptions are available by Razzaq and
Shazad (2004).
Material Examined
Pakistan: Khyber Pakhtunkhwa, District Mansehra, Khabbal
Paien, at 1825 m a.s.l., in groups, Aug. 2010, M. Fiaz, 21
(LAH100106); Dadar hills, at 1337 m a.s.l., solitary, Aug.
2010, M. Fiaz, FM31, (HUP Herbarium No. MFR–273),
(LAH100107).
Comments
Only
report
of
this
species
belongs
to
Karachi by
Razzaq and Shahzad in 2004. It is new record for district
Mansehra.
Scleroderma bovista Fr., Syst. Mycol. (Lundae) 3: 48 (1829)
(Figs. 3C and Fig. 10).
Basidiomata epigeous, 30 mm broad × 30 mm high,
globose to slightly subglobose, yellowish to dull brown,
with well-developed mycelial base. Peridium <1 mm
thick, tough, relatively rough, elastic, scales present;
scales black, thin, more dense on top, spot-like;
dehiscence by an irregular rupturing of an apical part.
Gleba firm, compact, powdery with age, grayish black.
Basidiospores dark brown, partially to completely
reticulate, ornamented, verrucose, 13–19 µm (av. 16 µm)
in diam. including ornamentation, 11–14.5 µm in diam.
excluding ornamentation, verrucae up to 4.7 µm high.
Exoperidium composed of hyaline, septate, branched
hyphae, up to 6 µm in diam. Mesoperidium composed of
hyaline, branched, septate hyphae with clamp
connections, up to 9.5 µm in diam. Endoperidium
composed of hyaline, thin walled, branched, septate
hyphae with clamp connections, up to 6 µm in diam.
Material Examined
PAKISTAN: Khyber PakhtunKhwa, Mansehra, 5 July.
2011, in groups, among grass, at a.s.l., M. Fiaz. 32,
(LAH100108).

Yousaf et al. / Int. J. Agric. Biol., Vol. 16, No. 3, 2014
576
Comments
It has been reported from Patriata (Murree hills) in 1956b by
Ahmad. It is a new record for District Mansehra.
Acknowledgements
This work was financially supported by Higher education
commission
(HEC) of Pakistan under the “Indigenous
Ph.D. Fellowship Scheme 5000 Batch VI”.
References
Ahmad, S., 1939. Higher Fungi of Punjab plains. II. The Gasteromycetes. J.
Ind. Bot. Soc., 18: 169–177
Ahmad, S., 1952a. Gasteromycetes of Pakistan. Publ. Dept. Bot. University
of the Punjab, 11: 1–92
Ahmad, S., 1952b. Gasteromycetes of West Pakistan. Punjab University
Press. Lahore
Ahmad, S., 1956. Fungi of Pakistan. Biol. Soc. Pak. Lahore, Monogr. 1: 1–
126
Ahmad, S., 1969. Fungi of Pakistan. Biol. Soc. Pak. Lahore, Monogr. 5: 1–
110
A checklist of gasteroid mycota of District Mansehra, Pakistan
Genus Species Habitat Distribution Literature
Astraeus
Morgan
Astraeus hygrometricus
(Pers.) Morgan, J.
Cincinnati Soc. Nat. Hist. 12: 20 (1889)
Growing under Pinus wallichiana
Kaghan Valley; Dadar,
Khabbal Paien (Mansehra)
Ahmad (1956)
Bovista Pers. Bovista plumbea Pers., Ann. Bot. (Usteri) 15
:
4 (1795)
Solitary to gregarious, among grass, on
ground
Batakundi (Kaghan
Valley); Musa-ka-
Musala
(District Mansehra)
Ahmad (1952,
1956)
Bovista polymorpha (Vittad.) Kreisel,
Reprium
nov. Spec. Regni veg. 69: 201 (1964)
On the ground, on soil Kaghan Valley
Ahmad (1952,
1956)
Crucibulum
Tul.
& C. Tul.
Crucibulum laeve
(Huds.) Kambly, Gast.
Iowa: 167 (1936)
On the ground Shogran (Kaghan Valley)
Ahmad (1952,
1956)
Geastrum Pers. Geastrum clelandii
Lloyd, Mycol. Writ.
5(Letter 53): 749 (1918)
on the ground Naran (Kaghan Valley)
Ahmad (1952,
1956)
Geastrum rufescens
Pers. [as 'Geaster'], Syn.
meth. fung. (Göttingen) 1: 134 (1801)
= Geastrum vulgatum Vittad.
On the ground Shogran (Kaghan Valley) Ahmad (1969)
Geastrum saccatum Fr., Syst. mycol.
(Lundae)
3(1): 16 (1829)
On the ground, solitary on sandy soil
among mix forest of Abies pindrow
Royle,
Picea smithiana (Wall.) Boiss and
Pinus
wallichiana A. B. Jackson
Shogran (Kaghan Valley),
Balakot
Ahmad (1956)
Geastrum schmidelii Vittad. [as 'Ge
aster'],
Monograph Lyc.: 12 (1842)
On the ground Shogran (Kaghan Valley) Ahmad
(1956b)
Geastrum triplex
Jungh. [as 'Geaster'],
Tijdschr. Nat. Gesch. Physiol. 7: 287 (1840)
On the ground, solitary to gregarious on soil
among mix forest of Abies pindrow Ro
yle,
Picea smithiana (Wall.) Boiss and
Pinus
wallichiana A. B. Jackson
Shogran (Kaghan Valley),
Balakot
Ahmad (1956),
Khan (1962)
Lycoperdon
Tourn. ex
Lycoperdon excipuliforme (Scop.) Pers.,
Syn.
meth. fung. (Göttingen) 1: 143 (1801)
On the ground, solitary to gregarious
Nathia gali, Musa Ka
Musala (district Mansehra)
Yousaf et al.,
2012
Lycoperdon oblongisporum
Berk. & M. A.
Curtis, in Berkeley, J. Linn. Soc., Bot. 10
(no.
46): 345 (1868) [1869]
On the ground Shogran (Kaghan Valley) Ahmad (1952)
Lycoperdon perlatum
Pers., Observ. mycol.
(Lipsiae) 1: 145 (1796)
On the ground, on soil, in groups, solitary
sometimes
Shogran, Sharan (Kaghan
valley), Khabbal Paien,
Ucharhi (District Mansehra)
Ahmad (1952,
1956)
Lycoperdon pratense Pers., Tent. disp.
meth.
fung. (Lipsiae): 7 (1797)
On the ground Kaghan Valley
Ahmad (1952,
1956)
Pisolithus
Alb.
& Schwein.
Pisolithus tinctorius (Mont.) E. Fisch., (1900)
On ground, among grass, solitary to
gregarious
Karachi; Khabbal Paien, Dadar
hills (District Mansehra)
Razzaq &
Shahzad (2004)
Phallus
L. ex
Pers
Phallus hadriani
Vent., Mém. Inst. nat. Sci.
Arts 1: 517 (1798)
On ground, among grass Mansehra
Phallus impudicus L., Sp. pl. 2: 1178 (1753) On soil
Batakundi, Shogran
(Kaghan Valley)
Ahmad (1952,
1956)
Phallus rubicundus (Bosc) Fr., Syst. mycol.
(Lundae) 2(2): 284 (1823)
On the ground, among grass
Balakot, Mahandri (Kaghan
Valley)
Ahmad (1939)
Rhizopogon Fr. Rhizopogon flavus
Petch, Ann. R. bot. Gdns
Peradeniya 6(3): 207 (1917)
Shogran, Sharan, Kaghan Ahmad (1956)
Scleroderma
Pers.
Scleroderma bovista
Fr., Syst. mycol.
(Lundae) 3(1): 48 (1829)
On the ground, among grass District Mansehra Ahmad
(1956), Khan
(1962)
Scleroderma flavidum
Ellis & Everh., J.
Mycol. 1(7): 88 (1885)
On the ground Shogran (Kaghan Valley) Ahmad (1956)
Scleroderma verrucosum
(Bull.) Pers., Syn.
meth. fung. (Göttingen) 1: 154 (1801)
On the ground Kaghan Valley
Ahmad (1952,
1956)
Secotium Kze. Secotium acuminatum
Mont., in Durieu, Expl.
Sci. Alg. 1(livr. 10): 371 (1848) [1846-49]
On the ground Shogran (Kaghan Valley) Ahmad (1956)

Gasteroid fungi of district Mansehra / Int. J. Agric. Biol., Vol. 16, No. 3, 2014
577
Ahmad, S., S. H., Iqbal and A.N. Khalid, 1997. Fungi of Pakistan. Sultan
Ahmad Mycological Society of Pakistan, Lahore
Bottomley, A.M., 1948. Gasteromycetes of South Africa. Bothalia, 4: 474–
810
Coker, W.C. and J.N. Couch, 1928. Gasteromycetes of the Eastern United
States and Canada. University of North Carolina Press, USA
Ellis, J.B. and M.B. Ellis, 1990. Fungi without gills: (Hymenomycetes and
Gasteromycetes): An identification Handbook, Chapman and Hal,
London
Kaewgrajang, T., U. Sangwanit, K. Iwase, M. Kodama and M. Yamato,
2013. Effects of Ectomycorrhizal Fungus Astraeus Odoratus on
Dipterocarpus Alatus Seedlings. J. Trop. Forest Sci., 25: 200–205
Khan, S.A. and M. Kamal, 1968. The fungi of South West Pakistan. Part I.
Pak. J. Sci. Ind. Res., 2: 61–80
Lans, C., N. Turner, T. Khan, G. Brauer and W. Boepple, 2007.
Ethnoveterinary medicines used for ruminants in British Columbia,
Canada. J. Ethnobiol. Ethnomed., 3: 11
Martin, T.P., 2001. Observations of mycorrhizal inoculation of pin and
scarlet oak production in containers, M.Sc. thesis. Blacksburg,
Virginia.
Miller, H.R. and O.K. Miller, 1988. Gasteromycetes: Morphological and
Developmental Features, with Keys to the Orders, Families, and
Genera, Eureka, Calif: Mad River Press
Mustafa, G., 2003. Mansehra, an introduction, gazetteer of the Hazara
District. Sang-e-Meel Publications, Lahore, Pakistan
Pegler, D.N., T. Laessoe and B. Spooner, 1995. British puffballs, earthstars
and stinkhorns, Royal Botanic Gardens, Kew
Pyasi, A., K.K. Soni and R.K. Verma, 2011. Dominant Occurrence of
Ectomycorrhizal Colonizer Astraeus hygrometricus of Sal (Shorea
robusta) in Forest of Jharsuguda, Orissa. J. Mycol. Plant Pathol., 41:
222–225
Ramesh, C. and M.G. Pattar, 2010. Antimicrobial properties, antioxidant
activity and bioactive compounds from six wild edible mushrooms
of Western Ghats of Karnataka, India. Pharmacognosy Res; 2: 107–
112
Razzaq, A. and S. Shahzad, 2004. Pisolithus tinctorius, a new record from
Pakistan. Pak. J. Bot., 36: 449–451
Shah, G.M. and M.A Khan, 2006. Check list of medicinal plants of Siran
Valley Mansehra–Pakistan. Ethnobot. Leaflets, 10: 63–71
SMEDA, NWFP. 2009. District profile Mansehra. Small and Medium
Enterprises Development Authority, Ministry of Industries and
Production. Government of Pakistan.
Turjaman, M., Y. Tamai, H. Segah, S.H. Limin, J.Y. Cha, M. Osaki and K.
Tawaraya, 2005. Inoculation with the ectomycorrhizal fungi
Pisolithus arhizus and Scleroderma sp. improves early growth of
Shorea pinanga nursery seedlings. New For., 30: 67–73
Yousaf, N., A.R. Niazi and A.N. Khalid, 2012. New records of noteworthy
gasteroid fungi from Pakistan. Mycotaxon, 119: 261–267
(Received 25 March 2013; Accepted 23 December 2013)