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Pogostemon cablin essential oil as feed additive promotes the repair of the rumen epithelial barrier in heat-stressed beef cattle
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Huan ChenI, Mingrui YangI, Xianglong ShangI, Hao ChenI, Yi LiI, Yanjiao LiI, Lin LiI, Mingren QuI, *, Xiaozhen SongI, *
Animal Nutrition | 2024, 18(1) : 433 - 440
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Animal Nutrition | 2024, 18(1): 433-440
• Original Research Article •
Pogostemon cablin essential oil as feed additive promotes the repair of the rumen epithelial barrier in heat-stressed beef cattle
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Huan ChenI, Mingrui YangI, Xianglong ShangI, Hao ChenI, Yi LiI, Yanjiao LiI, Lin LiI, Mingren QuI, *, Xiaozhen SongI, *
Affiliations
  • Jiangxi Province Key Laboratory of Animal Nutrition, Engineering Research Center of Feed Development, Jiangxi Agricultural University, Nanchang 330045, China
Published: 2024-09-10 doi: 10.1016/j.aninu.2024.06.001
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Pogostemon cablin essential oil (PEO), extracted from P. cablin, has anti-oxidant, anti-inflammatory, and anti-stress properties, as well as the ability to improve gastrointestinal digestion. This study aims to evaluate the effects of PEO on the performance, rumen epithelial morphology, and barrier function in heat-stressed beef cattle. Thirty-six male Jingjiang cattle at 18 months old were randomly assigned into four groups and fed a diet containing PEO at 0 (control), 50, 100, or 150 mg/kg in the feed concentrate (n = 9). All experimental cattle were fed under high temperature and humidity in summer for 60 days. The results indicated that 50 mg/kg of PEO treatment enhanced the average daily gain of beef cattle compared with the control group (P = 0.032). All PEO treatments reduced the diamine oxidase activity (P = 0.004) and malondialdehyde content (P = 0.008) in serum. In addition, the content of 70 kDa heat shock protein in the 100 mg/kg group was increased, and the activity of glutathione peroxidase and total antioxidant capacity in both 100 mg/kg and 150 mg/kg groups were enhanced compared to the control group (P < 0.05). More importantly, PEO treatment with 50 mg/kg enhanced the mRNA relative expressions of occludin in ruminal epithelia but decreased the mRNA relative expressions of c-Jun N-terminal kinase, P38 mitogen-activated protein kinases, caspase-3, Beclin1 (P < 0.05), and extremely significant declined the mRNA relative expressions of extracellular regulated protein kinases and ubiquitin-binding protein in contrast to the control group (P < 0.01). These findings indicated that dietary PEO supplementation might be favorable to improve growth performance and repairing damaged rumen epithelium of heat-stressed cattle by down-regulating the mitogen-activated protein kinase signaling pathway.

Beef cattle  /  Heat stress  /  Rumen epithelial barrier  /  Pogostemon cablin essential oil  /  Growth performance  /  MAPK signaling pathway
Huan Chen, Mingrui Yang, Xianglong Shang, Hao Chen, Yi Li, Yanjiao Li, Lin Li, Mingren Qu, Xiaozhen Song. Pogostemon cablin essential oil as feed additive promotes the repair of the rumen epithelial barrier in heat-stressed beef cattle[J]. Animal Nutrition, 2024 , 18 (1) : 433 -440 . DOI: 10.1016/j.aninu.2024.06.001
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1.　Introduction
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Heat stress caused by the hot environment in summer is becoming a major concern for pastoralists with the elevation of mean global temperature, especially in tropical and subtropical areas (St-Pierre et al., 2003). Reportedly, heat stress has been linked to reduced feed intake, antioxidant capacity, and nutrient digestion and utilization in beef cattle (Mader et al., 2006). The rumen is critical for nutrient and electrolyte absorption in ruminants; however, heat stress reduces the blood flow in the gastrointestinal tract, which may be harmful to the integrity of the rumen epithelium (Bernabucci et al., 2009). Heat stress injury may lead to a decrease in nutrient absorption efficiency, and pathogenic micro-organisms and their abnormal metabolites can enter the blood from the rumen and cause infection, suggesting a central role of the rumen in heat stress response in ruminants (Liu et al., 2013; Ma et al., 2021a,b; Zhai et al., 2019).
Pogostemon cablin essential oil (PEO) is an active ingredient derived from P. cablin (Blanco) Benth. (Labiatae) that is commonly used to treat vomiting, diarrhea, headache, and fever (Xu et al., 2021). P. cablin extract at 1 × 10−3 mg/mL can protect the follicular granulosa cells of hens from heat damage and maintain the normal secretory functions of the granulosa cells (Zhao et al., 2022). P. cablin essential oil plays a vital role in anti-oxidative and anti-inflammation processes (Wongsukkasem et al., 2018), and PEO by 90 μg/g DM in vitro culture may be responsible for modifying rumen fermentation ecology by improving ruminal feed degradability, microbial enzyme activities, and total protozoa counts (El-Zaiat and Abdalla, 2019). The main components of PEO include patchoulene, patchouliol, pogostone, etc. Patchouliol and pogostone are the active ingredients. Pogostone has shown anti-colorectal tumor effects in human colorectal carcinoma hct116 cells by inducing autophagy and apoptosis involving phosphoinositide 3-kinase/protein kinase B/mammalian target of rapamycin (PI3K/Akt/mTOR) axis (Cao et al., 2017). These results suggested that PEO has the potential to improve ruminal fermentation and maintain a stable rumen environment in ruminants. However, it is not clear what the effects of PEO are on ruminant heat stress and rumen epithelial barrier. We hypothesized that PEO might improve the growth performance by promoting the repair of the rumen epithelial barrier in heat-stressed beef cattle. Therefore, the present study was designed to test this hypothesis.
2.　Materials and methods
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2.1.　 Animal ethics statement
Jiangxi Agricultural University's Committee for the Care and Use of Experimental Animals approved this trial (JXAU-2020-40).
2.2.　 Preparation of PEO products
P. cablin essential oil (purity of 98%, contains 27.38% patchouliol, 19.25% α-patchoulene, 15.23% α-guaiene, etc.) was obtained from Jiangxi Zhongcheng Pharmaceutical Co., Ltd, Jiangxi province (China). The process of making the powder was completed by Hangzhou King Techina Feed Co., Ltd. (Hangzhou, China), and the contents of PEO in the final PEO products were 60%, and the remaining components are β-cyclodextrin inclusion agents.
2.3.　 Animals and experimental design
Thirty-six healthy male Jinjiang cattle of 18 months of age at a weight of 330 ± 21 kg were kept indoors in individual pens with concrete floors. Following a 10-day adaptation period, the feeding trial lasted 60 days (from July 11 to September 8 in 2022). Throughout the trial period, all cattle were allocated randomly to one of four treatments and dietary with 0 (control), 50, 100, and 150 mg/kg PEO products (n = 9). Table 1 shows the composition and nutrient levels of the basal diet. NEmf was calculated according to the Chinese Feeding Standard of Beef Cattle (NY/T 815-2004). Dry matter (DM) content was detected by the National Standard of China (GB/T 6435-2014) using a constant temperature oven, and crude protein (CP) content was determined by standard GB/T 6432-2018 using an automatic Kjeldahl apparatus (HGK-50, Shanghai Heguan, China). Neutral detergent fiber (NDF) and acid detergent fiber (ADF) contents were determined by standards GB/T 20806-2022 and NY/T 1459-2022, respectively, using an automatic fiber analyzer (ANKOM 200, USA). Calcium content was determined using the potassium permanganate titration method (GB/T 6436-2018) and total phosphorus was determined by standard GB/T 6437-2018 using a dual beam UV visible spectrophotometer (TU-1901, Beijing Puxi, China). There were no antibiotics in the diets. The PEO products were premixed in the concentrate and then evenly mixed with brewer grains (wet, moisture 79.25%) and rice straw (3 to 5 cm length). Diets were supplied to the cattle twice daily at 06:00 and 17:00 and leftover materials collected 1 h after each feeding. Fresh water was available for ad libitum consumption throughout the study. The body weight of animals on an empty stomach was measured at 09:00 at the beginning and end of the trial, and the daily feed intakes were recorded during the experimental period. Based on these data, average daily dry matter intake (ADMI), average daily gain (ADG), and the ratio of feed and gain (F/G) were calculated.
2.4.　 Detection of the temperature-humidity index (THI)
The temperature and humidity index was calculated from air temperature and relative humidity according to the method of Herbut et al. (2018). The air temperature and relative humidity in the cowshed at 08:00, 14:00 and 20:00 each day were determined using a thermohygrometer according to methods described by a previous study (Peng et al., 2021).
2.5.　 Serum parameters analysis
On day 60, blood sampling (15 mL each) was obtained from cattle by jugular vein puncture, and then serum was obtained by centrifugation (3000 × g, 10 min, 4℃) and then stored at −20℃ for assay. The diamine oxidase (DAO) activity, 70 kDa heat shock protein (HSP70) content, and lipopolysaccharide (LPS) content in serum were measured following the manufacturer's recommendations when utilizing Enzyme linked immunosorbent assay (ELISA) kits from Solarbio Science & Technology (Beijing, China). The total antioxidant capacity (T-AOC), activities of total superoxide dismutase (T-SOD), glutathione peroxidase (GSH-Px), and the content of malondialdehyde (MDA) in serum were measured using spectrophotometric kits (Nanjing Jiancheng Bioengineering Institute, Nanjing, China). The contents of interleukin-6 (IL-6), interleukin-1β (IL-1β), interferon-γ (IFN-γ), and tumor necrosis factor-α (TNF-α) in serum were analyzed using ELISA kits (Nanjing Jiancheng Bioengineering Institute, China).
2.6.　 Rumen epithelial tissue sample collection and preparation
Eight cattle from the control and 50 mg/kg PEO groups (four individuals per therapy with medium body weight) were chosen as experimental cattle for rumen epithelial tissue sample collection based on the performance and serum indices results. At the end of this trial, these cattle were transported to a slaughterhouse approximately 500 m away and slaughtered according to standard procedures. All contents were quickly removed from the rumen, and one rumen wall piece measuring 2 cm × 2 cm was cut using surgical scissors from the abdominal sac, and then they were rinsed in ice-cold sterile phosphate buffer solution (pH 7.4). The rumen tissue samples were divided into three pieces: one of the samples was chopped into smaller pieces (approximately 1 g) and frozen in liquid nitrogen for quantitative real-time PCR, and the other two pieces for histomorphological examination were cut into 1 cm × 1 cm and 0.5 cm × 0.5 cm pieces and put in 4% polyformaldehyde and 2.5% glutaraldehyde solutions for scanning electron microscopy and paraffin sections, respectively.
2.7.　 Pre-staining and electron microscopy of rumen epithelial tissue sections
Rumen epithelial tissue sections for light microscopy and electron microscopy analysis were prepared using methods previously described by Liu et al. (2013). The 40 × objective lens was used to measure each stratum, and five photos were recorded per papilla for a total of 10 replicates per measurement per animal. The thickness of total epithelium (TE), stratum corneum (SC), stratum granulosum (SG), and stratum spinosum and basal (SSB) in the rumen wall were measured by Image-Pro Plus software (version 6.0, Media Cybernetics Inc., Bethesda, MD, USA). The papillae were dried to a critical point using liquid CO2 as a medium, then mounted and gold-coated for scanning electron microscopy. The samples were observed with scanning electron microscopy (Hitachi Model S-3000N, Hitachi Technologies, Tokyo, Japan).
2.8.　 Quantitative real-time PCR (RT-qPCR)
Quantitative real-time PCR was used to quantify the relative expression of tight junction proteins, apoptosis and autophagy, mitogen-activated protein kinase (MAPK) signaling pathway-related genes at the mRNA relative expression levels. The ruminal samples were extracted for total RNA, and the cDNA was reverse-transcribed using the cDNA Synthesis Supermix Kit (TransGen Biotech, Beijing, China). Quantitative real-time PCR was conducted via the Green qPCR SuperMix Kit (TransGen Biotech, Beijing, China) and CFX96 Touch Real-Time PCR System (Bio-Rad Inc., Hercules, CA, USA) according to the following specifications: 95℃ for 10 min, 45 cycles at 95℃ for 15 s, 60℃ for 60 s, and extension at 95℃ for 15 s, which were the RT-qPCR profiles. All samples were examined three times. The 2−ΔΔCt method was used to calculate the relative expressions of these genes, with β-actin serving as the housekeeping gene. Primer 5.0 software was used to design amplification primers for all genes, displayed in Table 2.
2.9.　 Statistical analysis
The data are presented as mean and standard deviation (SEM). The SPSS 19.0 statistical software's one-way ANOVA method was used to analyze growth performance and serum parameters (Windows; SPSS, Chicago, USA). The ruminal morphological parameters and protein variables (mRNA relative expression levels) between the control and 50 mg/kg groups were compared using the SPSS 23.0 independent sample t-test. P < 0.05 was used as the significance level, and a trend was set at 0.05 < P < 0.10.
3.　Results
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3.1.　 Temperature humidity index, growth performance
As shown in Fig. 1, the values of average daily THI during the whole trial period were higher than 79, of which 35 days were above 84. Moreover, the data in Table 3 showed PEO treatment with 50 mg/kg increased the ADG of beef cattle (P = 0.032), and tended to enhance their ADMI compared with the control group (P = 0.081). As the PEO levels increased, ADG (P = 0.047) and ADMI (P = 0.042) increased quadratically.
3.2.　 Blood index
As presented in Table 4, PEO treatment with 100 mg/kg enhanced the content of HSP70 (P = 0.010), PEO at 50 mg/kg tended to decrease the content of IL-1β ( P = 0.090), and all treatments reduced the DAO activity and MDA content in serum (P < 0.05). Also, there was an increasing trend for the activity of T-SOD in the 50 mg/kg group ( P = 0.065) and GSH-Px activity and T-AOC were enhanced in the 100 and 150 mg/kg groups when compared to the 0 mg/kg (control) group (P < 0.05). With an increase in PEO level, HSP70 content (P = 0.012) and GSH-Px activity (P = 0.006) and T-AOC (P = 0.007) increased linearly, however, the DAO activity (P = 0.017; P = 0.007) and MDA content (P = 0.029; P = 0.006) declined linearly and quadratically, respectively.
3.3.　 Histomorphological parameters
P. cablin essential oil treatment at 50 mg/kg decreased the ruminal SC's thickness compared with the control group (P = 0.007, Table 5). Moreover, the rumen papillae of the control group showed a state of desquamation, cracking, and excessive keratinization, whereas in the 50 mg/kg group, the surface of the papillae was repaired and keratinization was not obvious (Fig. 2).
3.4.　 The mRNA expression of tight junction proteins in the ruminal epithelium
In Fig. 3A, 50 mg/kg dietary supplementation with PEO increased the mRNA expression of occludin in ruminal epithelium compared with the control group (P = 0.035).
3.5.　 Effects of PEO on apoptosis and autophagy in heat-stressed beef cattle ruminal epithelium
As presented in Fig. 3B and C, compared to the control group, 50 mg/kg dietary supplementation with PEO decreased the mRNA expression of caspase-3 (CAS, P = 0.029), ubiquitin-binding protein (P62, P < 0.001) and Beclin1 (BEC, P = 0.033) in ruminal epithelium compared with the control group. Meanwhile, the 50 mg/kg PEO group reduced the average optical density of CAS (P = 0.010) and P62 (P = 0.029) as shown in Table 6.
3.6.　 The mRNA expression of MAPK signaling pathway-related genes in the ruminal epithelium
In Fig. 3D, 50 mg/kg dietary supplementation with PEO decreased the mRNA relative expressions of c-Jun N-terminal kinase (JNK, P = 0.017), extracellular regulated protein kinases (ERK, P < 0.001), and P38 mitogen-activated protein kinases (P38, P = 0.013) in ruminal epithelium compared with the control group.
4.　Discussion
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The THI is used to evaluate the occurrence of heat stress among cattle. The critical values for minimum, mean, and maximum THI were 74 ≤ THI ≤ 79, 79 ≤ THI ≤ 84, and ≥84, respectively (Herbut et al., 2018). In this study, the THI was above 79 during the whole period, which indicated that the experimental cattle were in a state of heat stress and as a consequence the feed intake and growth performance were decreased (Mader et al., 2006). The current results indicated that dietary supplementation with 50 mg/kg PEO increased the ADG and tended to increase ADMI, and ADG and ADMI increased quadratically with the increase of the PEO level. These results suggested that dietary with PEO alleviated the heat stress response of beef cattle. This may be related to the effect of P. cablin, the source of PEO, commonly used to treat heat stroke. Consistently, our previous reports showed dietary supplements with Chinese medicine preparations containing P. cablin could increase the ADG and DMI of beef cattle (Chen et al., 2020). Animal heat tolerance was positively correlated with the concentration of HSP70, which is sensitive to temperature, is involved in cell development, and can protect animals from heat stress (Bagatell et al., 2000; Wang et al., 2017). The current results indicated that the content of HSP70 in serum increased linearly, suggesting PEO may contribute to the heat tolerance of beef cattle.
Although little research exists on the effect of patchouli oil against heat stress of animals, numerous studies have shown that patchouliol and pogostone could improve anti-oxidative and anti-inflammatory properties (Lin et al., 2014; Dechayont et al., 2017). In this investigation, PEO treatment linearly enhanced the T-AOC and GSH-Px activity in serum and decreased the content of MDA in serum linearly and quadratically, which suggested that PEO was important in anti-oxidative stress. High ambient temperature can induce High environmental temperatures can induce oxidative stress in farm animals (Bernabucci et al., 2014). A similar result in vitro showed that patchouli alcohol, the main component of PEO, modulated the morphology of IEC-6 cells and reduced their oxidative stress responses to heat shock (42℃ for 3 h) (Liu et al., 2016). Another study has demonstrated that supplementing with patchouli oil enhanced the activities of glutathione reductase (GR), GSH, and SOD in liver of animals under oxidative stress, which was in line with our results (Huang et al., 2018).
Additionally, heat stress can cause dysfunction or inflammation in animals, such as increased serum inflammatory cytokines and white blood cell count, and intensify inflammation (Tao et al., 2012). In this study, the serum content of IL-1β in the 50 mg/kg group tended to decrease. These results suggested that PEO inhibited the inflammatory response, which may be due to a single or synergistic effect of the essential oil's main components (including patchoulol, a-bulnesene and a-guaiene) or other minor constituents (such as seychellene and a-patchoulene) (Silva-Filho et al., 2016). A previous study on rats has shown that PEO and its derived compounds can reduce the concentration of inflammatory cytokines (Leong et al., 2019).
The rumen epithelium, which is made up of the stratum corneum, granular layer, spinous process layer, and basal layer, serves as a primary physical barrier to keep toxic substances in the rumen from infecting the rumen epithelium cells (Kleen et al., 2003). A previous study has demonstrated that oxidative stress induces inflammation and apoptosis of keratinized cells, leading to injury of the rumen epithelium (Ma et al., 2021a,b). In this study, supplementation with PEO reduced the thickness of SC in the rumen, suggesting PEO as a feed additive could repair damaged rumen epithelium of heat-stressed cattle. Scanning electron microscopy results consistently showed that PEO treatment improved rumen epithelial abscission and hyperkeratosis. Moreover, the current study showed that PEO decreased the activity of serum DAO linearly and quadratically. Diamine oxidase, which is found in the epithelial villus, may be released into blood vessels as the gastrointestinal epithelium's integrity deteriorates (Wu et al., 2018). The preceding outcomes indicated that adding PEO repaired the damaged rumen epithelium and improved the integrity of the rumen epithelium in heat-stressed beef cattle. Similarly, several studies on rats have shown that supplementing with PEO can improve gastrointestinal tract injury and protect the integrity of the gastrointestinal tract epithelial barrier (Chen et al., 2014; Liu et al., 2017).
A network of tight junctions and junction-associated proteins maintains the rumen epithelial barrier (Aschenbach et al., 2019). Tight junction proteins such as claudin, ZO-1, and occludin are essential in rumen epithelial barrier integrity. A previous finding showed that stress caused a decrease in mRNA expression of tight junction proteins, resulting in the disruption of tight junction structures (Hashimoto et al., 2008). The current results showed that supplementation with PEO increased the levels of occludin mRNA relative expression. The above results indicated that diets with PEO could repair the damage to the rumen epithelial barrier caused by heat stress, which is consistent with the results of antioxidant and anti-inflammatory PEO treatment. A similar finding showed that PEO significantly enhanced the mRNA relative expression of ZO-1 and occludin, and improved intestinal barrier function in rats (Leong et al., 2019).
Heat stress usually induces the production of ROS, and oxidative stress occurs when intracellular ROS cannot be eliminated as quickly as possible (Houston et al., 2018). Some studies have found that ROS can activate MAPK pathways, resulting in inflammation, apoptosis and cell death, then giving rise to tissue damage (McCubrey et al., 2006; Torres and Forman, 2003; Cargnello and Roux, 2011). In general, cell apoptosis is controlled by genes to maintain a stable internal environment, with key genes being BEC and BCL2-associated X (BAX). Previous studies have reported that various toxic agents cause apoptosis in multiple tissues, including the liver and kidney, by increasing cytochrome c, BAX, and CAS levels and decreasing BEC levels, resulting in severe damage to tissues (Küçükler et al., 2021; Thangarajan et al., 2018). Autophagy is another physiological event induced by oxidative stress; moreover, BEC, microtubule-associated protein 1 light chain 3 (LC3) and P62 are involved in the autophagic process, which are essential markers used to determine the degree of autophagy. Furthermore, a previous study showed that autophagy activation protects against multiple tissue injuries under various stress conditions (Mo et al., 2018). It has been reported that natural antioxidant resveratrol reduced the abnormal reactive oxygen species accumulation, reducing autophagy and apoptosis in ovarian tissues (Jiao et al., 2022). A previous study determined that RUT (rutin, a flavone derivative) treatment protected against liver and kidney damage by attenuating VPA-induced (valproic acid) oxidative stress, endoplasmic reticulum stress, inflammation, apoptosis and autophagy (Kandemir et al., 2022).In the presented study, RT-qPCR and immunofluorescence results showed that PEO addition decreased the mRNA relative expression levels of CAS, P62 and BEC, which inferred that PEO protected against apoptosis and autophagy, and it is consistent with previous results from scanning electron microscopy and paraffin sections.
The MAPK are a highly conserved family of serine/threonine kinases that play a central role in the range of fundamental cellular processes like cell growth, proliferation, death, and differentiation, including JNK, ERK1/2, and P38. Thus, ERK1/2 activation regulates cell proliferation. In the meantime, JNK and P38 are stress-responsive proteins that participate in inflammatory and apoptotic responses, respectively (Cargnello and Roux, 2011; Zhou et al., 2021). A previous study has confirmed that platycodon grandiflorum saponins (PGS) treatment protected against heat stress-induced oxidative injury in testis tissues by decreasing phosphorylation of JNK, ERK, and P38 MAPK (Leng et al., 2019). Another report showed that PIF_9 (pterostilbene derivative, a homolog of natural polyphenolic product of resveratrol) could block LPS-induced phosphorylation of ERK, JNK, and P38, which relieves oxidative stress (Fang et al., 2021). However, in our research, the 50 mg/kg PEO treatment group decreased the mRNA relative expressions of MAPK signaling pathway-related genes and the content of MDA. Still, it tended to increase the GSH-Px activity, T-AOC, SOD activity compared with the control group, which indicates that PEO treatment protected against heat stress-induced oxidative injury in the rumen epithelial tissue by reducing the expression levels of JNK, ERK, and P38 MAPK, which was consistent with the previous rumen epithelial tissue sections results. Nevertheless, the specific molecular mechanisms will need to be investigated further.
5.　Conclusion
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In conclusion, dietary supplements with PEO alleviated heat stress response, improved antioxidant status and immunity, and PEO at 50 mg/kg promoted the repair of the rumen epithelial barrier and improved beef cattle growth performance in hot conditions.
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Year 2024 volume 18 Issue 1
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Article Info
doi: 10.1016/j.aninu.2024.06.001
  • Receive Date：2023-03-12
  • Online Date：2026-01-28
  • Published：2024-09-10
Article Data
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History
  • Received：2023-03-12
  • Revised：2024-05-23
  • Accepted：2024-06-11
Affiliations
    Jiangxi Province Key Laboratory of Animal Nutrition, Engineering Research Center of Feed Development, Jiangxi Agricultural University, Nanchang 330045, China

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Corresponding authors. E-mail addresses: (M. Qu)
(X. Song).
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表12种不同金属材料的力学参数
科
Family		 属数
Number of
genus		 种数
Number of
species		 占总种数比例
Percentage of
total species (%)		 属
Genus		 种数
Number of
species		 占总种数比例
Percentage of total
species (%)
鹅膏菌科Amanitaceae 2 11 5.26 鹅膏菌属 Amanita 10 4.78
小菇科 Mycenaceae 2 12 5.74 丝盖伞属 Inocybe 5 2.39
多孔菌科 Polyporaceae 8 14 6.70 蜡蘑属 Laccaria 5 2.39
红菇科 Russulaceae 3 23 11.00 小皮伞属 Marasmius 6 2.87
小菇属 Mycena 11 5.26
光柄菇属 Pluteus 5 2.39
红菇属 Russula 17 8.13
栓菌属 Trametes 5 2.39
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