Comparative nutrient composition of selected wild edible mushrooms from two agro-ecological zones, Uganda

Over 2,500 different mushrooms grow in the wild around the world and their nutritional potential has long been overshadowed by the well known cultivated mushrooms such as Lentinus edodes, Pleurotus species and Agaricus bisporus. A high biodiversity of wild mushroom biota is found throughout the tropics, particularly sub-Saharan Africa, with about 300 edible mushroom species (Harkonen et al. 1995; Rammeloo and Walleyn 1993). Many of these fungi belong to the genus Termitomyces, with a symbiotic relationship with termites (Heim 1958). Termitomyces are said to be superior to all other mushrooms globally because of their biting aroma (Singer 1962). Several ethnic groups of tropical countries consume wild mushrooms (Chang and Mshigeni 2001; Van Dijk et al. 2003; Nakalembe et al. 2009). In Uganda, several mushroom species such as Armillaria mellea, Lentinus prolifer, Termitomyces aurantiacus, Termitomyces eurrhizus and Termitomyces microcarpus among many others grow in most parts of the country (Katende et al. 1999; Nakalembe et al. 2009). Most of these wild mushrooms are reportedly used for food, medicine, cultural festivals and to some extent for income generation (Nakalembe et al. 2009). However, their nutritional value has never been adequately studied and documented. The objective of this investigation was to determine and compare some nutrient composition of five mushroom species obtained from two agro-ecological zones of Mid-Western Uganda.

The substrate, mushroom species, age and part of the basidiomata as well as mushroom storage conditions after harvest are one of the factors that affect mushroom chemical composition (Adejumo and Awosanya 2005). More still, results of the same species of mushrooms obtained by different investigators may be different due to the influence of different techniques of analysis involved. Therefore, the data generated by other investigators can only be used to produce estimates of probable nutritive value of given mushroom species.

Generally, this study indicates that the studied mushrooms are good sources of proteins, crude fiber, carbohydrates, vitamins and minerals. Mushrooms from humid zone had high concentration of nutrients, which may have been contributed by the acidity and organic matter content of the soil (Colak et al. 2009). Furthermore, different species of mushrooms had variable amount of nutrients probably because of species/strain differences and their ability to bioaccumulate the minerals and other nutrients into their tissues (Mattila et al. 2001; Mshandete and Cuff 2007).

High dry matter contents observed in these mushrooms is due to lowered moisture contents, which would otherwise affect the concentration of soluble solids that make up the dry matter. Moisture variation may have been caused by a series of factors such as the environmental factors during growth and storage; and the relative amount of metabolic water produced during storage (Mattila et al. 2001). The moisture and dry matter values were comparable with previously reported data in Uganda (Opige et al. 2006; Kabasa et al. 2006).

In this study, large amounts of total carbohydrates are contained in the dry matter of mushrooms, which is consistent with the values reported for wild mushrooms in other parts of the world (Sanmee et al. 2003; Gbolagade et al. 2006; Saiqa et al. 2008). It constitutes of the chitin, polysaccharides (β-glucans) and sugar alcohols (Kurtzman 1997; Mattila et al. 2001). A considerable amount of this carbohydrate is dietary fiber that would serve as roughage with low calorific value. The presence of sugar alcohols makes these mushrooms substitutes for the high energy sugar in diabetic patients (Hamano 1997).

Bernaś et al. (2006) observed that differences in protein contents could be due to species/strain specific, the growth substrate, pileus size, time of harvest and the level of nitrogen available in the growth substrate. The content of protein varied between 17.58 and 27.43% on a dry weight basis for P. tenucuilus (sub-humid) and T. microcarpus (humid region) making up to 35.2–54.9% of 50 g of protein/day of Recommended Daily Intake (RDI), which is within the average value of 19–35% dry weight for dried mushrooms (Crisan and Sands 1978). These results are in accordance with those in literature (Sanmee et al. 2003), and well below other documented values of some wild mushrooms (Adejumo and Awosanya 2005; Chye et al. 2008; Colak et al. 2009; Palazzolo et al. 2012). As compared to the staple foods; 7.3% rice, 12.7% wheat, 9.4% maize, these mushrooms contain much more protein, and therefore, mushroom protein can supplement the low protein diets of poor people who cannot afford animal resource foods.

The total fat content was low, varied from 2.015 to 3.79% dry weight (3.1–5.83% RDI of 65 g of crude fat/day). Mushrooms obtained from humid areas had the highest fat content 2.995–3.79%. However, the fat content was within the range of the reported value of wild mushrooms i.e. 1.1–8.1% on dry weight basis (Crisan and Sands 1978), and slightly lower than wild mushrooms of Eastern Uganda (3.868–4.491% dry weight) (Opige et al. 2006). In this study, crude fat content is comparable to that of millet (2.8%) and maize (4.2%) (FAO 1972). Mushroom fat is reportedly low but rich in essential unsaturated fatty acids which are considered essential for human diet and health.

Crude fiber is also part of a healthy diet. It was within the reported value of 3–35% fiber on a dry weight basis (Breene 1990) and ranged between 2.084–9.46% (8.34–37.84% RDI, *25 g of fiber/day). Compared with cereals and vegetables, mushrooms are as good as cereals but with high fiber value compared to some vegetables e.g. carrots (0.6%) and lettuce (0.2%) (FAO 1972). The results of this study concur with crude fiber values of cultivated mushroom species elsewhere, for instance, 7.3–9.3% for Coprinus, 7.5–16.3% for Pleurotus (La Guardia et al. 2005) and 5.5–17.4% for Volvariella species (Aletor 1995). However, Chye et al. (2008) recorded high crude fiber content of some of the wild mushrooms such as P. tenuiculus (39.85%). Since the mushroom species examined contained significant amounts of crude fiber, they could be regarded as good sources of dietary fiber for supplementation of some foodstuffs with less fiber such as vegetables, hence utilized as roughage, and mostly its immune-stimulation effects should not be overlooked.

Energy values of the studied wild mushrooms were low and dependant on both mushroom species and the source (Table 1). They varied from 220.75 to 266.14 kcal/100 g dry weight providing only 11.04–13.31% of the RDI of 2,000 kcal/day. The energy values are slightly below that of cereals (millet 341 kcal and maize 349 kcal) (FAO 1972). Other studies done elsewhere reported relatively high energy values of wild mushrooms ranging from 367.9–450.2 kcal/100 g (Mshandete and Cuff 2007; Colak et al. 2009). Taking this into consideration, mushrooms can be used for weight management.

Like many other organisms, mushrooms bioaccumulate several minerals from their growth media with the help of its greater part, the mycelia. The latter has the highest growth rate, is compressed in nature and is spread over areas of several square metres (Eurola et al. 1996). These facilitate its efficiency extraction of nutrients from the growth media and bioaccumulate them in relative quantities. However, mineral concentrations in fungi may depend on several interdependent factors namely the climate, season of the year, state of maturity, basidiomata part as well as storage conditions after harvest (Varo et al. 1980; Adejumo and Awosanya 2005).

Ash in edible fungi ranges from 5 to 13 g/100 g dry matter (Varo et al. 1980) with the major minerals constituting about 56–70% of the total ash content (Li and Chang 1982). Potassium accounts for nearly 45% of the total ash content. In this study, the ash content of mushrooms ranged between 11.2 and 16.9% for humid areas while 10.79–13.82% for sub-humid. Other studies reported relatively higher ash content (Wardlaw and Kessel 2002) while others very low as small as 2.45% for P. tenuiculus and 2.00% for Lycoperdon perlatum (Colak et al. 2009). The wild mushrooms under study were more deficient in major minerals than trace elements especially in Na, Ca and Mg. Potassium and phosphorus were the predominant elements among the major minerals. This is in line with other studies done elsewhere in the world (Mattila et al. 2001; Barros et al. 2008; Chye et al. 2008; Colak et al. 2009; Palazzolo et al. 2012). Potassium ranged from 1809.7 to 3354.45 mg/100 g making 38.4–71.4% RDI of 4,700 mg/day and P ranged from 508 to 840 mg/100 g (51–84% RDI, 1,000 mg/day). The contents of K were high compared to Na; an important attribute from the nutritional point of view as it is a main electrolyte and major cation inside the cell. Phosphorus content was high in contrast to some Nigerian wild mushrooms (2.3–29.8 mg/100 g; Gbolagade et al. 2006) and very low in T. microcarpus of Uganda (156.53 mg/100 g; Nabubuya et al. 2010) on dry weight basis. Phosphorus is essentially required by all cells in the body for normal functioning (Knochel 1999). It is efficiently absorbed from the gastrointestinal tract and available in most foods, hence less important in diet planning (Wardlaw and Kessel 2002).

Magnesium (7.14–31.9 mg/100 g) was low contributing about 1.8–8.0% of RDI of 400 mg/day. Magnesium was found to be as low as 0.5–1.6 mg/100 g dry weight in ectomycorrhizal mushrooms (Sanmee et al. 2003) on dry weight basis. However, their contents in this study are slightly low in some wild mushrooms (0.4–6.7 mg/100 g, Gbolagade et al. 2006) but too low compared to green vegetables, legumes and whole grain cereals (100–500 mg/100 g), meat and dairy products (100–300 mg/100 g) (FAO 1972). Therefore, this requires a combination of the latter foods together with these mushrooms in order to obtain adequate magnesium for proper functioning of the body.

Furthermore, Ca and Na levels were also quite low in these mushrooms contributing only 1.1–1.6% and 0.4–0.7%, respectively of the RDIs. In contrast, the sodium contents reported elsewhere are as low 0.28 mg/100 g dry weight basis (Mattila et al. 2001). However, low Na concentrations are of great benefit nutritionally to the consumer, especially in hypertensive patients (Feldman et al. 1986). Mattila et al. (2001) reported insignificant levels of Ca in cultivated mushrooms ranging from 0.05 to 0.25 g/kg dry weight, and very low in ectomycorrhizal mushrooms (Sanmee et al. 2003). Calcium content (10.6–15.5 g/100 g) in this study was in agreement with other studies (Gbolagade et al. 2006), higher than in other studies carried out in Uganda (0.0095–0.0115%, Olila et al. 2008) and very low compared to other values (77–144.7 mg/100 g) elsewhere in the world (Chye et al. 2008). However, it was comparable to many common vegetables (10.0–52.0 mg/100 g) (FAO 1972), and lower than the recommended daily intakes in all age groups (Food and Nutritional Board 2001, 2004). Its low content in mushrooms suggests a low intake of Ca in vegetarians; therefore supplementation is required to meet their Ca requirements.

Among the trace elements, Se content was higher (120–148 µg/100 g) than other trace elements, as well as the recommended FAO daily intake (55 µg/100 g). Sanmee et al. (2003) reported Se contents of ectomycorrhizal mushrooms as extremely low to very high (0–12,600 µg/100 g); whereas cultivated mushrooms had a value between 0.33 and 320 µg/100 g. About 70 and 50 µg of Se were suggested as sufficient daily requirement for men and women, respectively (Food Nutrition Board 2000); whereas Yang et al. (1988) proposed 600 and 400 µg as the daily maximum and safe intake of dietary selenium, respectively. This proves that the studied mushrooms are safe for human consumption. Selenium is an essential nutrient required for prevention and treatment of several conditions including cardiomyopathy, fatigue and keep the keratinized tissues normal (Kumar 1995) in addition to being a powerful antioxidant (Charanjeet et al. 2003).

Iron content (10.6.6–22.7 g/100 g) was above the RDI (18 mg/day) as well as the upper level intake (40–45 mg/day) (Food and Nutrition Board 2001), higher than the published value for cabbage (6 mg/kg) and that of those sources considered nutritionally dense in Fe such as meat (16 mg/kg) (Eyabi 2001). The Fe content is quite higher than the tolerable upper intakes (40–45 mg/day). Iron content in these wild mushrooms is line with other studies done on wild mushrooms (Zakhary et al. 1983; Chye et al. 2008; Colak et al. 2009), but higher than in other studies (0.07–0.09 mg/100 g, Gbolagade et al. 2006). However, this total Fe content may not constitute an accurate guide to confirm the levels in this resource, but its bioavailability, which also depends on its form, the needs of the body and the presence or absence of antinutritional factors that may influence its absorption. However, it was observed that mushrooms contain insignificant levels of phytates, which would otherwise affect its bioavailability (Colak et al. 2009). Despite this, one should take care when consuming mushrooms in combination with other foods such as vegetables that may influence absorption of Fe.

Fe was followed by Mn ranging from 0.25 to 1.19 mg/100 g (12.5–60% RDI, 2 mg), a value within that of bread and cereals (0.68–9 mg/kg) and slightly lower than in eggs, milk and meat (<1 mg/kg); and green vegetables (2 mg/kg) (Pelkonen et al. 2008). Mn content in this study concur with other studies (Gbolagade et al. 2006), but it can be as high as 14.3 mg/100 g (Colak et al. 2009). Pelkonen et al. (2008) recommended 12 mg/day as an acceptable intake for the general public, suggesting that consumption of these mushrooms may not cause any intoxication to humans. Manganese is an important element in the body as it is a cofactor of enzymes and an antioxidant.

Copper is the third most abundant trace mineral in the body, and helps protect the cardiovascular, skeletal, and nervous systems. It ranged between 0.2 and 0.75 mg/100 g of copper, a value lower than the recommended daily intake (2 mg/day). However, this value is adequate for all age groups, except in pregnancy and lactation which require 1 mg/100 g of Cu (Food and Nutritional Board 2001). In contrast, other studies in Uganda indicated high copper content (Kabasa et al. 2006; Nabubuya et al. 2010) as well as in other parts of the world (Chye et al. 2008; Colak et al. 2009).

Zinc content was low in all mushroom species ranging from 0.56 to 1.1 mg/100 g (3.7–7.3% RDI, 15 mg), hence, very low for all age groups (Food and Nutrition Board 2001). Zinc concentrations were lower than in most meats (10–50 mg/kg), whole grain cereals (10–20 mg/kg) and milk (3 mg/100 g) (Pelkonen et al. 2008). Cellular metabolism involving immune function, protein synthesis, wound healing, DNA synthesis and cell division requires zinc (Heyneman 1996).

Vitamins contributes a very small percentage of food in our diet daily, but important in prevention of diseases and longevity (Olaniyi 2000). In this study, the wild edible mushrooms exhibited a good profile of vitamins, particularly thiamin, niacin, folic acid and vitamin C, as it was observed in other studies elsewhere (Mattila et al. 2001; La Guardia et al. 2005). Pantothenic acid, biotin and vitamin B₁₂ were not detected in any of the mushroom species that were studied. Alpha-tocopherol was also not identified in T. globulus. The vitamin contents in this study were lower than what was obtained in fresh wild mushrooms (Chye et al. 2008); suggesting losses of these vitamins during mushroom handling such as drying. Vitamin concentrations in mushrooms may also be affected by several factors such as climatic conditions, strain of mushroom, stage of harvest, storage and handling of the mushroom samples during analysis.

The mushrooms contained high folic acid content, an essential vitamin in the maintenance of good health, treatment and prevention of anemic diseases (Refsum et al. 1998). Folic acid is one of the commonest deficiencies seen worldwide. It has been found to affect several groups of people including women on oral contraceptives, pregnant mothers, elderly, alcoholics and children are affected by its deficiency. In this study, folic acid content (70–380.3 µg/100 g) is adequate for all age groups except in pregnancy and lactation (500–600 μg/day) (Food and Nutritional Board 2001). This value is almost of the same magnitude as that generally found in some vegetables, higher than that of fruits (3–23 μg/100 g) (FAO 1972) and lower than in other wild mushrooms (1,222–1,412 μg/100 g dry weight) (Bano and Rajarathnam 1988). Fortunately, folic acid bioavailability in mushrooms is good compared to some vegetables, such as peas and spinach (Clifford et al. 1991).

Vitamin C contents were in moderate amounts (11.05–21.40 mg/100 g), contributing 14.7–28.5% of the recommended FAO/WHO (2005) daily intake of 75 mg/day. This value is adequate for children and very low for other groups of people (Food and Nutritional Board 2001). Due to its antioxidant and therapeutic properties, vitamin C is a valuable food component (Bernaś et al. 2006). The results of this study were quite higher than the range of the reported values in other mushroom species (Lau et al. 1985). However, vitamin C contents in these mushrooms concur with other reports elsewhere (Barros et al. 2008); and comparable to that of fruits and vegetables (FAO 1972). In contrast, Opige et al. (2006) found no detectable vitamin C in T. microcarpus. Although ascorbic acid contents varied considerably among the five types of wild edible mushrooms analyzed, these mushrooms could serve as a source of vitamin C in the diet.

These mushrooms showed considerable amounts of niacin (2.13–7.31 mg/100 g), providing only 10.7–36.6% of the recommended daily value (20 mg/day). The niacin value is within the RDI for children, but very low for other groups of people ((Food and Nutritional Board 2001). The mushrooms had high niacin contents comparable to eggs (0.8–4.4 mg/100 g), but lower than in meat (7.5–11.6 mg/100 g). These values are higher than those in vegetables and fruits (FAO 1972).

Thiamin content ranged between 0.05 and 0.94 mg/100 g (3.47–62.7%, RDI of 1.5 mg/day), relatively higher than those contained in fruits (0.02–0.07 mg/100 g) and eggs (trace-0.04 mg/100 g) but comparable to vegetables (0.01–0.12 mg/100 g), cereals (0.29–0.33 mg/100 g) (FAO 1972) and cultivated mushrooms (Mattila et al. 2001). These mushrooms provide adequate thiamin content to all groups of people except in pregnancy and lactation (Food and Nutritional Board 2001). Riboflavin content was low and ranged between 0.06 and 0.09 mg/100 g, making only 2.9–5.3% of the RDI (1.7 mg/day). It was slightly higher than that of fruits (0.01–0.05 mg/100 g, FAO 1972) but within the range of other mushrooms (Furlani and Godoy 2008), common vegetables (0.01–0.3 mg/100 g), and most common cereals (0.11–0.18 mg/100 g) (FAO 1972).

Beta carotene content was low (12.60–17.70 μg/g dry weight) but within the range of other reported ß-carotene values in wild mushrooms (2.52–75.48 µg/g dry weight, Barros et al. 2008). Chye et al. (2008) reported higher concentration of ß-carotenes in Malaysia’s wild mushrooms ranging from 0.37 to 2,711 μg/g fresh weight suggesting a loss of this vitamin during drying. However, cultivated mushrooms are reported to have lower concentrations (7.24 μg/g) than the mushrooms in this study. β-carotene is an important antioxidant required for stimulating the growth of new skin cells (Shukkit-Hale et al. 2006; Elmastas et al. 2007).

In addition to ß-carotene, these mushrooms were found to contain trace amounts of α-tocopherol ranging from 0.39 to 0.52 μg/100 g dry weight. Alpha tocopherol is the most active component of the vitamin E complex and a powerful antioxidant of the human body (Burton and Ingold 1989). The mushrooms lacked biotin, vitamin B₁₂ and pantothenic acid, which observation is in disagreement with other reports elsewhere (Breene 1990; Mattila et al. 2001).

Generally, the five mushroom species studied irrespective of their sources are good sources nutrients and compare favorably with the most common green leafy vegetables, legumes, whole grain cereals, meats and dairy products. In Uganda and indeed in other developing countries, micronutrient deficiency is the main cause of death and poor performance due to the poor staple foods consumed. This affects mainly the children, women, HIV-AIDs patients and the elderly. Therefore, if these mushrooms are encouraged to be consumed together with the common staple foods, especially of a poor man’s diet, stand a high chance of solving malnutrition in the above mentioned vulnerable groups of people.