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Article
Peer-Review Record

Updating Ecology and Distribution of Wild Truffles in Morocco

Forests 2023, 14(5), 952; https://doi.org/10.3390/f14050952
by Fatima Henkrar 1,*, Chaimae Meyad 1,2, Marwa Oikrim 1,2, Nezha Bouhaddou 3 and Lahsen Khabar 2,*
Reviewer 1: Anonymous
Reviewer 2:
Reviewer 3: Anonymous
Forests 2023, 14(5), 952; https://doi.org/10.3390/f14050952
Submission received: 14 March 2023 / Revised: 28 April 2023 / Accepted: 3 May 2023 / Published: 5 May 2023
(This article belongs to the Special Issue Truffle Hunting and Mushrooms Ecology in Forest Ecosystems)

Round 1

Reviewer 1 Report

This article reports some climate, soil and vegetation data related with desert truffles distribution in Morocco. 

 

However, the authors fail to present new information due to the lack of the annual mean of the total production recorded for all harvested truffle species. 

 

Authors should clarify the following points:

 

Abstract 

- line 14: “parameters affecting..” is too general, change to “climatic and soil parameters relating..”

- line 20: what is the growth period? Have the authors studied other climatic parameters? 

- lines 22-23: Explain the sentence “T. boudieri, T. claveryi and especially Tirmania spp require(s) less than 100 mm in high CaCO3 percentage”. According to table 3, the annual average precipitation is always more than 100 mm for all sites. The CaCO3 is given in g/kg not percentage in table 4.

 

Introduction 

- line 42: is T. oligospermum appreciated by the Spanish or the Italian people?

- line 43: which Italian truffle do the authors mean?

- line 47: change Boudieri for boudieri

- line 63: to which species do you refer with “This underground mushroom grows”? is it singular or plural?

- Explain why the authors do not mention a very similar previous study of their own from one of the study sites (Bioecology of desert truffles in the province of Figuig in Eastern Morocco, in Scientia Fungorum 2017). 

 

Materials and methods 

- line 92: indicate when the regular surveys for collections of truffles were held: during how many and what years, in which months, periods and how often during the period. 

To obtain meaningful results, several years should be sampled and the production of each year at each site should be recorded. If the harvest has only been done for one year, this work is not valid because it is not representative.

- line 93: the presence of truffles is a qualitative parameter, not a quantitative one. It would be necessary to give quantities of truffles collected (kg/m2 in the areas of 100 m2 of study) for the article to be meaningful and interesting. At least the frequency of occurrence percentages should be given. 

- line 93: explain how the area-species saturation curve was done

- line 101: Indicate how many soils samples/area were done.

- line 106: For how many years were the periodical outings made to determine the plants?

- line113: how the R studio was applied to the climatic data?

 

Results and discussion

- line 145: Helianthemum guttatum has passed into synonymy and has been reclassified as Tuberia guttata, it should be changed throughout the text.

-line 148 and table 2: Currently Tuber asa has been identified as Tuber gennadi, otherwise explain how to distinguish T. asa from T. gennadi.

- Table 2: what does maturation period mean?

- lines 218-227: the results can not be compared to those obtained by Bradai et al. (2015) since annual variation of desert truffle production in relation to precipitation amounts is not calculated here.

- Figure 4 is not informative; the authors do not provide statistical data of the effects of climate parameters on desert truffle species specific and total productivities in the different areas of Morocco. Therefore, their conclusions on the effect of climate on the distribution of desert truffle species are speculative and not demonstrative.

- What importance or interest do the non-host plants have in the occurrence or distribution of desert truffles in the different zones?

- A correspondence analysis should be done to obtain comparisons of truffle composition and soil characteristics between all sites.

 

The conclusions are very general and hardly add anything new to what is already known about truffle ecology in Morocco.

 

There are several grammatical errors related to the verb tenses depending on whether it is singular or plural, they should be checked throughout the manuscript.

Author Response

Dear Reviewer, Thank you for the reviewers’ comments concerning our manuscript. Those comments are all valuable and very helpful for revising and improving our paper, as well as the important guiding significance to our researches. We have studied comments carefully and have made correction. Please find the revised version of our manuscript.

Abstract 

- Point 1: “parameters affecting..” is too general, change to “climatic and soil parameters relating..”

Response 1: modified

 

Point 2: what is the growth period? Have the authors studied other climatic parameters? 

Response 2: the fructification and abundance depend on precipitation

 

Point 3: Explain the sentence “T. boudieri, T. claveryi and especially Tirmania spp require(s) less than 100 mm in high CaCO3 percentage”. According to table 3, the annual average precipitation is always more than 100 mm for all sites. The CaCO3 is given in g/kg not percentage in table 4.

Response 3: rectified in the text

 

Introduction 

Point 4: is T. oligospermum appreciated by the Spanish or the Italian people?

Response 4: by spanish and italian, but we delate it from the text. We focused more on ecology instead of socio-economy

 

Point 5: which Italian truffle do the authors mean?

Response 5: Tuber borchii

 

Point 6: change Boudieri for boudieri

Response 6: modified

 

Point 7: to which species do you refer with “This underground mushroom grows”? is it singular or plural?

Response 7: plural

 

Point 8: Explain why the authors do not mention a very similar previous study of their own from one of the study sites (Bioecology of desert truffles in the province of Figuig in Eastern Morocco, in Scientia Fungorum 2017). 

Response 8: added

 

Materials and methods 

Point9: indicate when the regular surveys for collections of truffles were held: during how many and what years, in which months, periods and how often during the period. 

Response 9: the period added in text

 

Point 10: To obtain meaningful results, several years should be sampled and the production of each year at each site should be recorded. If the harvest has only been done for one year, this work is not valid because it is not representative.

Response 10: We add the yield for economic species according to several years production in tons/year

Point 11: the presence of truffles is a qualitative parameter, not a quantitative one. It would be necessary to give quantities of truffles collected (kg/m2 in the areas of 100 m2 of study) for the article to be meaningful and interesting. At least the frequency of occurrence percentages should be given. 

Response 11: We insert the quantities of truffles collected (kg/m2 in the areas of 100 m2 of study).

 

Point 12: explain how the area-species saturation curve was done

Response 12: delated from the text

 

Point 13: Indicate how many soils samples/area were done.4

Response 13: we added the number of samples in text

 

Point 14: For how many years were the periodical outings made to determine the plants?

Response 14: from 2014 to 2021

 

Point 15: how the R studio was applied to the climatic data?

Response 15: R Studio was used to perform climatograph using ggplot2

 

Results and discussion

Point 16: Helianthemum guttatum has passed into synonymy and has been reclassified as Tuberia guttata, it should be changed throughout the text.

Response 16: modified

 

Point 17: Currently Tuber asa has been identified as Tuber gennadi, otherwise explain how to distinguish T. asa from T. gennadi.

Response 17: We added in the text T. asa/gennadi

 

Point 18: what does maturation period mean?

Response 18: Maturity period, modifed

 

Point19: the results can not be compared to those obtained by Bradai et al. (2015) since annual variation of desert truffle production in relation to precipitation amounts is not calculated here.

Response 19: modified

 

Point 20: is not informative; the authors do not provide statistical data of the effects of climate parameters on desert truffle species specific and total productivities in the different areas of Morocco. Therefore, their conclusions on the effect of climate on the distribution of desert truffle species are speculative and not demonstrative.

Response 20: The figure 4 gives an idea about the precipiation and temperature fluctuation for each month. It informe about the average rainfull amount nad T° acquired before and during maturity period mentionned in Table 2. Especially that Table 3 shows only the annual average and there is no monthely rainfull and T° average.

 

Point 21: What importance or interest do the non-host plants have in the occurrence or distribution of desert truffles in the different zones?

Response 21: Removed from the table 3. The non host plants are also important, some of them are intermediary plants that mycorrhize with desert truffles such as Cistus spp. While others, preserve humidity and shadow for truffle environnement.

Point 22: A correspondence analysis should be done to obtain comparisons of truffle composition and soil characteristics between all sites.

Response 22: We didn’t do truffles compositions

 

Point 23: The conclusions are very general and hardly add anything new to what is already known about truffle ecology in Morocco.

Response 23: modified

 

Best regards

Author Response File: Author Response.docx

Reviewer 2 Report

Dear Authors
it was a pleasure to go though your paper but major revision must be considered. In general, your material and methods must be improved and you need to focus on the ecological aspects of truffle distribution rather than consider socio-economic implication, which you can use for the conclusion. Moreover, the approach you use must be deeply revise because you report several results unlinked the methods. Here after i report a sent of specific passages of your paper that should be improved.

Row 33: you started immediately addressing the desert truffle. I suggest to introduce the paper with a more general overview of truffle ecology in Morocco.

Row 37-46, 49-50: is it an ecological paper or economic one? Please, remove the economic reference at the paper. You can address to the economic aspects in the conclusions. I suggest to start the introduction from the row 51.

Row 63: I suggest to use “hypogeal fungi” instead “underground mushrooms”

Row 92-94: it is not clear the method you applied to select the areas. Please provide evidences.

Row 106-108: how did you collected truffle?

Row 252: try to avoid the use very abundant or other subjective adjectives, without specifying a reference area or level. 659 mm might be considered abundant in some area and very low in others.

Row 253: Tuber aestivum var. aestivum and Tuber aestivum var. uncinatum are two varieties of the same species.

Row 255-258: sentence without contextual means

Row 267-270: the reference is meaningless in the context of the paper. You highlighted the same conclusion on your paper. Please rephrase the sentence: Our findings confirm the conclusion of ….

Row 287-289: You refer to the productivity, but in the paper, there is no evidence on how you measured. You should describe the concept in material and methods as well in the results.

Looking forward on your improved paper

Best regards

 

Author Response

Dear Reviewers, Thank you very much for the reviewers’ comments concerning our manuscript. Those comments are all valuable and very helpful for revising and improving our paper, as well as the important guiding significance to our researches. We have studied comments carefully and have made correction. Please find the revised version of our manuscript.

Please find the point-by-point response for your comments:

Point 1: you started immediately addressing the desert truffle. I suggest to introduce the paper with a more general overview of truffle ecology in Morocco.

Response 1: modified in text

 

Point 2: is it an ecological paper or economic one? Please, remove the economic reference at the paper. You can address to the economic aspects in the conclusions. I suggest to start the introduction from the row 51.

Response 2: modified and the socioeconomic part delated from the introduction

 

Point 3: I suggest to use “hypogeal fungi” instead “underground mushrooms”

Response 3: modified

 

Point 4: it is not clear the method you applied to select the areas. Please provide evidences.

Response 4: rectified

 

Point 4: how did you collected truffle?

Response 5: added in the text

 

Point 5: try to avoid the use very abundant or other subjective adjectives, without specifying a reference area or level. 659 mm might be considered abundant in some area and very low in others.

Response 5: modified

 

Point 6: Tuber aestivum var. aestivum and Tuber aestivum var. uncinatum are two varieties of the same species.

Response 6: modified

 

Point 7: Row 255-258 sentence without contextual means

Response 7: delated from the text

 

Point 8: Row 267-270: the reference is meaningless in the context of the paper. You highlighted the same conclusion on your paper. Please rephrase the sentence: Our findings confirm the conclusion of ….

Response 8: modified

 

Point 8: Row 287-289: You refer to the productivity, but in the paper, there is no evidence on how you measured. You should describe the concept in material and methods as well in the results.

Looking forward on your improved paper

Response 7: modified in the Material and methods and we add the production Kg/m2 in the table 2.

 

Best regards

Author Response File: Author Response.docx

Reviewer 3 Report

1.     I suggest writing Tuber aestivum instead of Tuber uncinatum/aestivum in the abstract and in the whole document.

 

2.     I suggest to differentiate in all text "desert truffles" than "truffles" to avoid confusion for the reader. Example (In L43-L45): What species of truffles is concerned like "Moroccan truffles"? "Dessert truffles", "truffles" or both groups.

 

3.     Line 42-43: It is necessary to clarify which two species of Italian truffles you are talking about.

 

4.     The ecological study of the environment is not clear at all. It is necessary to clarify in much more detail how you have carried out the sampling. For each of the 8 sites: how many plots did you use? what kind you sampled (mycorrhizae, carpophores,...)? how did you collected these samples? how many samples did you collect for each type of sample (mycorrhizae, carpophores,...)? It is also necessary to describe how you determined the composition of the vegetation in each plot.

 

5.     L 212-216:"Terfezia arenaria, in Mamora forest requires a maximum rainfall of 250 mm on average before March, while other Terfezia spp. require a rainfall amount less than 200 mm for a good harvest. A decrease in rainfall with a slight rise in temperature during the ripening period (March-May) is also necessary. Adequate temperature values during this period are 14 to 18°C." In this sentence, clarify how you arrived at this conclusion? the data results is not shown.

 

6.     In Figure 5, I think there is an error in the rainfall scale? It ranges from 0 to 800. Would it be from 0 to 80?

7.     In the conclusions, you talk about Tuber melanosporum. But on the other hand, you don't say anything in the whole document.

Author Response

Dear Reviewers, Thank you very much for the reviewers’ comments concerning our manuscript. Those comments are all valuable and very helpful for revising and improving our paper, as well as the important guiding significance to our researches. We have studied comments carefully and have made correction. Please find the revised version of our manuscript.

Please find the point-by-point response to your comments:

1.     I suggest writing Tuber aestivum instead of Tuber uncinatum/aestivum in the abstract and in the whole document.

 Response 1: accordingly modified in text

2.     I suggest to differentiate in all text "desert truffles" than "truffles" to avoid confusion for the reader. Example (In L43-L45): What species of truffles is concerned like "Moroccan truffles"? "Dessert truffles", "truffles" or both groups.

Response 2: Moroccan truffles are both truffles belonging to Tuber spp. and desert truffles

3.     Line 42-43: It is necessary to clarify which two species of Italian truffles you are talking about.

Response 3: Tuber oligispermum is mixed with italian truffles Tuber borchii. But we remove the socioeconomic part from the introduction, focusing more on ecology only.

 

4.     The ecological study of the environment is not clear at all. It is necessary to clarify in much more detail how you have carried out the sampling. For each of the 8 sites: how many plots did you use? what kind you sampled (mycorrhizae, carpophores,...)? how did you collected these samples? how many samples did you collect for each type of sample (mycorrhizae, carpophores,...)? It is also necessary to describe how you determined the composition of the vegetation in each plot.

Response 4: all those informations are now added in the Materiel and methods (revised version)

 

5.     L 212-216:"Terfezia arenaria, in Mamora forest requires a maximum rainfall of 250 mm on average before March, while other Terfezia spp. require a rainfall amount less than 200 mm for a good harvest. A decrease in rainfall with a slight rise in temperature during the ripening period (March-May) is also necessary. Adequate temperature values during this period are 14 to 18°C." In this sentence, clarify how you arrived at this conclusion? the data results is not shown.

Response 5: This is got from an other study and we add the reference in the text.

6.     In Figure 5, I think there is an error in the rainfall scale? It ranges from 0 to 800. Would it be from 0 to 80?

Response 6: Yes, thank you for mentioning this. It was an error. During writing the script in R studio, we multiply by mistake the scale of Temperature*8. That’s why, it became 800. Now it is rectified in the revised figure.

 

7.     In the conclusions, you talk about Tuber melanosporum. But on the other hand, you don't say anything in the whole document.

Response 7: Yes, because Tuber melanosporum is not native species in Morocco. It was introduced by a producer and his own plantation in Immouzer Kandar and Debdou. This T. melanosporum is frach origine, but he succeed in producing truffles. We add this information in the conclusion and we insert also the annual production of this species also.

 

 

Best regards

Author Response File: Author Response.docx

Round 2

Reviewer 1 Report

- In the new version (lines 89-90), the study area is 3 plots of 100 m2 in each of the sites, however, in the 1st version it was 1 plot of 100 m2 in each site, please clarify.  

 

- Indicate whether the truffle production (average number of carpophores) in Table 2 corresponds to the average of the 8 years of study (2014-2021).

 

- Table 2: the average amount of carpophores in table 2 is very low, better expressed in g rather than kg.

Explain why this production is so low considering that it is the average of 8 years.

Indicate whether the potential host plants are with all fungal species at each site or not, it is not clear from the table 2.

 

- The authors do not answer how to distinguish Tuber asa from Tuber gennadii, it is wrong to write T. asa/gennadii.

 

Tuber asa would be a rather rare species, with very few collections and very poorly interpreted. The specimen preserved in the Mattirolo herbarium, sent by Ferry de la Bellone, was revised by Trappe in 1968 and determined as Delastreopsis oligosperma (=Tuber oligospermum). T. asa is a species that has been confused with T. gennadii.

Authors should check these articles and decide on the correct name:

 

Alavarez IF, Parlade J & Trappe JM (1992) Loculotuber gennadii gen. et comb. nov. and Tuber multimaculatum sp. nov. Mycologia, 84 (6): 926-929.

 

Agnello C & Kounas V (2021) Tuber asa and T. gennadii. A close morphological study of two species often confused in the past with a brief historical bibliographic summary. Ascomycete.org 3 (4): 65-74.

 

- The authors do not discuss in the text the production obtained in relation to the climatic variables analyzed in the study areas during the 8 years, they only comment on the article by Bradai et al (2015). To affirm that precipitation is important, the authors have to make new graphs relating desert truffle yields (g/m2) to precipitation, during the different years, as in Fig. 4 of the article by Bradai et al (2015).

 

Likewise, a PCA analysis should be done to obtain comparisons of truffle production and soil characteristics between all sites, that gives more robustness to the comments of the discussion in this aspect.

 

Author Response

Response to Reviewer #1 comments

- Point 1: In the new version (lines 89-90), the study area is 3 plots of 100 m2 in each of the sites, however, in the 1st version it was 1 plot of 100 m2 in each site, please clarify.  

 

Response 1: We would like to thank the reviewer for addressing the following remark. In the first version, we wrote that "a minimum area of about 100 m2 for all plant species", we didn't specify how many plot we took.

 

- Point 2: Indicate whether the truffle production (average number of carpophores) in Table 2 corresponds to the average of the 8 years of study (2014-2021).

 

Response 2: We would like to thank the reviewer for addressing the following remark. The average amount of carpophores correspond to 8 years and we modified in the table 2.

 

- Point 3: Table 2: the average amount of carpophores in table 2 is very low, better expressed in g rather than kg.

Explain why this production is so low considering that it is the average of 8 years.

Indicate whether the potential host plants are with all fungal species at each site or not, it is not clear from the table 2.

 

Response 3: We would like to thank the reviewer for addressing the following remark. The average amount is very low because the surface is small as well, it is in Kg/m2. We convert it in g/m2. For example 95g/m2 of Terfezia arenaria is 9.5 Kg/100m2. In addition, These values are not a sum total of 8 years, it is an average of the 8 years.

 

- Point 4: The authors do not answer how to distinguish Tuber asa from Tuber gennadii, it is wrong to write T. asa/gennadii.

 

Tuber asa would be a rather rare species, with very few collections and very poorly interpreted. The specimen preserved in the Mattirolo herbarium, sent by Ferry de la Bellone, was revised by Trappe in 1968 and determined as Delastreopsis oligosperma (=Tuber oligospermum). T. asa is a species that has been confused with T. gennadii.

Authors should check these articles and decide on the correct name:

 

Alavarez IF, Parlade J & Trappe JM (1992) Loculotuber gennadii gen. et comb. nov. and Tuber multimaculatum sp. nov. Mycologia, 84 (6): 926-929.

Agnello C & Kounas V (2021) Tuber asa and T. gennadii. A close morphological study of two species often confused in the past with a brief historical bibliographic summary. Ascomycete.org 3 (4): 65-74.

 

 Response 4: Thank you for pointing out this relevant remark. There is always confusion between the Tuber asa and Tuber gennadii. Here is the photos of ascospores observed in our laboratory.

 

According to ascospores description of Agnello C & Kounas V (2011), the ascospores are ellipsoid or citriform (eye-shaped), indicatiing that the species found is Tuber gennadii, not Tuber asa. But according to Astier J. (1998), the same description is for Tuber asa. Please see photo bellow of the Astier (1998).

 



We modified the species name in the manuscript according to the recent publication of Agnello C & Kounas V (2011). Please see Table 2 and line 153. In addition, we mentionned in the line 112-113 that the descrimination of Tuber asa and Tuber gennadii was done following Agnello C & Kounas V (2021) description, where they specified that the asci of Tuber gennadii contains 2 ascospores. We are sure that it is not Tuber oligospermum, because this species is collected under Helianthemum guttatum, and the morphological critereas does’nt much with Tuber asa or Tuber gennadii.

 

- Point 5: The authors do not discuss in the text the production obtained in relation to the climatic variables analyzed in the study areas during the 8 years, they only comment on the article by Bradai et al (2015). To affirm that precipitation is important, the authors have to make new graphs relating desert truffle yields (g/m2) to precipitation, during the different years, as in Fig. 4 of the article by Bradai et al (2015).

 

Response 5: We would like to thank the reviewer for pointing out this relevant remark. We establish an analysis of production in relation to the precipitation during 8 years. Please see the Figure 5.

 

- Point 6: Likewise, a PCA analysis should be done to obtain comparisons of truffle production and soil characteristics between all sites, that gives more robustness to the comments of the discussion in this aspect.

 

Response 6: Thank you for pointing out these relevant remarks. We do agree that PCA analysis should be done to obtain comparisons of truffle production and soil characteristics. We do the PCA analysis for that, please see Figure 6.

Author Response File: Author Response.docx

Reviewer 2 Report

Hi

well done. Just few changes and the paper is done. I listed the minor changes that i suggest to have the paper ready:

Row 47-48: remove "and the west of the Arab world

Row 121: not clear, please rephrase these part of the sentence “November to May 2014 to 2021”

Ros 412-416: please remove. There is an embargo on seedling supply from third country in Morocco.

Looking forward on your paper published

Cheers

 

Author Response

We would like to thank the reviewer for your positive feedback.

 

- Point 1: Row 47-48: remove "and the west of the Arab world.

 

Response 1: We would like to thank the reviewer for addressing the following remark. We removed this sentence from the text.

 

- Point 2: Row 121: not clear, please rephrase these part of the sentence “November to May 2014 to 2021”

 

Response 2: Thank you for pointing out this relevant remark. We removed The word November to May, because it create the confusion.

 

- Point 3: There is an embargo on seedling supply from third country in Morocco.

 

Response 2: Thank you as well for this remark. But, there is no sentence saying “There is an embargo on seedling supply from third country in Morocco” in our manuscript.

 

Author Response File: Author Response.docx

Reviewer 3 Report

Dear authors,

Now, it is better understood how the sampling has been done, although for future works I recommend you to improve it.

Best regards.

 

 

Author Response

Response: We would like to thank the reviewer for the positive feedback.

 

Best regards.

Author Response File: Author Response.docx

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