Tree diversity in agroforestry systems of native fine-aroma cacao, Amazonas, Peru.

Cocoa cultivation is of considerable economic and social importance to the Amazonas region and is commonly associated with forest species in the region. However, the diversification level and composition of cacao agroforestry systems in Peru are poorly understood. The objective of this study is, therefore, to describe the diversity of tree species in cocoa AFS by plantation age. Accordingly, the number of species of 15 plots covering a total of 1.5 hectares was recorded. Moderately low levels of tree species diversity were reported (H´ ranged 0.89-1.45). In total 17 species were reported throughout the study area. The most abundant botanical family was represented by a single Musa sp. species. The dissimilarity indices show a moderate similarity between the age ranges evaluated (over 62%). Additionally, the IVI indicates that the most important species are used for food and timber apart from providing shade, additionally major of this species are introduced intentionally for the farmers. Based on the observations, it may be concluded that the farmer's interest in obtaining further benefits from the plot, mostly economic benefits affect the diversification of cocoa agroforestry systems.

Introduction

Cocoa (Theobroma cacao L.) is one of the main crops grown in agroforestry systems (AFS) by smallholder farmers in humid tropics [1]. The installation of cocoa farms occurs mainly by partially clearing forests; the retained trees provide shade for cocoa and coproduction channels to farmers, while leaf mulch from shade trees and nutrients stored in the forest soil ensure productivity [2, 3].

Cocoa AFS is a socio-economically viable system in which farmers intentionally integrate shade trees, cocoa, and food crops together on the same plot [4]. Organic cocoa AFS uses a variety of shade trees to both suppress weed growth and insect pests outbreaks [5, 6] and compensate for nutrient loss due to nutrient uptake by cocoa trees through nitrogen fixation, reduction of nutrient leakage and decomposition of shade tree litter [6].

Cocoa AFS conserve the diversity of native plants and animals [7] and provide products that diversify farmers’ diets. It generates supplemental income and some security from climate change-related shocks [1, 8, 9]. Moreover, cocoa trees benefit from an improved microclimate and increased water retention [1, 5, 10]. Therefore, cocoa cultivation in AFS is an alternative to contribute significantly to the mitigation of biodiversity loss and ecosystem resilience in tropics regions [9, 11], especially within areas where forest cover has been significantly reduced [12]. Furthermore, it has been shown that an integration of organic agriculture and agroforestry would effectively enhance biodiversity conservation [9, 13].

However, there is a growing global demand; and despite the current challenging economic and geopolitical world situation in the first half of the 2021/2022 season, the cacao demand sustained a positive stance and the prices also sustained this hike [14]. This would lead to farmers putting even more pressure on cocoa-producing ecosystems, which along with the scarcity of information to support the above claims and the importance of tree diversity in cocoa agro-ecosystems would worsen conservation and recovery of disturbed areas.

In the Amazonas region, there are no studies yet that show the diversity of trees associated with cocoa cultivation; therefore, the present work aims to identify the species present within the AFS and measure the Diameter at Breast Height (DBH). These data allowed to obtain: 1) The diversity, abundance and importance value of shade trees within the system; 2) The composition and spatial distribution of trees in the AFS of cocoa in the Amazon.

Materials and methods

Study area

The study was carried out in cocoa AFS belonging to members of the APROCAM Multiple Service Cooperative. The APROCAM cooperative consists of 235 small producers distributed in 4 districts in the province of Bagua (Aramango, Copallín, La Peca and Imaza), 2 districts in the province of Utcubamba (Cajaruro and El Parco) and 1 district in the province of Santa María de Nieva (Nieva) in the Amazonas. The climate in the area is warm tropical with an average temperature of 25°C and annual rainfall between 500–1500 mm.

Data collection methods

In the aforementioned territories, 15 plots were selected (Fig 1) according to the age of the crop. The plots were grouped into three strata (young cocoa AFS: 8–15 years; middle-aged cocoa AFS: 16–29 years and old cocoa AFS: 30–40 years); these three age groups were determined because cocoa reaches its peak production at 8 years of age and stabilizes until 15 years of age, from 16 to 30 years of age cocoa production is maintained on average and finally after 30 years of age the yield declines modernly and becomes an adult cocoa with a low yield [16, 17]. In addition, each of the farms selected were at least 1.5 ha in size.

Fig 1

Plot location map.

Map prepared by the authors based on open access resources: political-administrative boundaries from geoBoundaries [15], local details of ARA-Amazonas (http://visor.regionamazonas.gob.pe/indexv.php) and ALOS PALSAR digital elevation model (https://search.asf.alaska.edu/#/), 28 of June 2022.

Data collection was carried out from November to December 2020. In each selected plot, a 50 m x 20 m rectangular subplot (sample) was established and the number of species within this subplot was recorded. In total, an area of 1.5 ha of cocoa cultivated area was sampled.

Tree species were identified at the field itself, since the trees found (fruit and timber species) were widely known by technicians. On the contrary, for species where it was not possible to taxonomically identify, only the common name provided by farmers and a botanical sample were taken for later identification. This botanical identification was carried out with the help of specialized bibliography and expert consultation in the KUELAP-UNTRM herbarium (Campus Universitario: C. Universitaria N° 304, Chachapoyas, Amazonas, Perú). Additionally, the recognized species were classified as native or exotic according to their origin; and as forest, medicinal or timber species according to their main use by farmers or potential products.

The Circumference at Breast Height (CBH) of each of the stems of the tree species including cocoa trees was taken at 1.3 m above the ground. This data was transformed into Diameter at Breast Height (DBH) of each of the measured stems. For this transformation we used “π” as a circumference division factor.

Data processing and analysis

Diversity of shade trees

The data obtained were processed with PAST 3 software to generate a diversity analysis. For each plantation and age range, species richness (S) and the effective number of species (N) indices were calculated, as well as Shannon (H’), Simpson (1-D), Margalef (Dmg) [18], and Chao-1 indices [19]. Excel spreadsheets were used to manage tables and graphs, such as the Venn diagram for species richness.

The Importance Value Index was estimated using the following formula developed by Curtis and McIntosh [20]:

Where: RA: is relative abundance calculated as the number of individuals per species. RF: is relative frequency estimated as the proportion of plots where the species occurred at least once. RD: is relative dominance defined as the basal area per species per hectare.

Composition and spatial distribution of trees in the cocoa agroforestry system

To evaluate the species composition in each age range, the Jaccard and Sorensen indices were used [18]. In addition, the trees were grouped according to their potentially usable products (wood, fruit, or medicinal). The basal area of all shade species and cocoa trees was also established.

Statistical analysis

All data that conformed to ANOVA assumptions were processed using this analysis to establish differences between age groups. All analyses were performed using Infostat v.2020 software and at a significance level of 5% (p<0.05) [21].

Results

Diversity, abundance, and importance value

A total of 454 individuals distributed in 14 families were inventoried in this study (Table 1). Only two families exceeded 50 individuals being the most abundant (Musaceae and Boraginaceae). In general, when visualizing the merged data for species per botanical family (Table 1), the families with the highest species richness are Anacardiaceae (2 species), Fabaceae (2 species), and Rutaceae (4 species). It is also observed that the highest number of shade tree individuals was inventoried in the youngest plots (8–15 years old) with 206 individuals.

Table 1

Number of species and abundance of individuals by botanical family in each age range of AFS and as a total.

	Young		Middle-aged		Old		Total
Familia	Spec.	Indiv.	Spec.	Indiv.	Spec.	Indiv.	Spec.	Indiv.
Anacardiaceae	2	2	1	3	1	2	2	7
Annonaceae	1	2	0	0	0	0	1	2
Arecaceae	1	1	1	3	0	0	1	4
Malvaceae	0	0	0	0	1	2	1	2
Boraginaceae	1	14	1	29	1	12	1	55
Caricaceae	0	0	0	0	1	5	1	5
Fabaceae	2	7	1	8	2	8	2	23
Lauraceae	1	2	1	5	1	5	1	12
Meliaceae	1	3	1	1	1	3	1	7
Musaceae	1	167	1	63	1	86	1	316
Rubiaceae	1	3	0	0	1	2	1	5
Rutaceae	3	5	2	3	3	8	4	16
Total	14	206	9	115	13	133	17	454

Species richness was the lowest at middle aged (16–29 years) cacao plots (Table 2). In fact, there were a total of 17 species observed in the study. The estimated total number of species based on Chao-1 was 15, 9.5 and 15 for young cocoa AFS, middle-age cocoa AFS, and old cocoa AFS respectively. Simpson’s (1-D) and Shannon’s (H) indices ranged from 0.34 to 0.63 and 0.89 to 1.45 respectively. In general, in the study area, middle-age AFS are the least diverse compared to young and old AFS (Table 2).

Table 2

Diversity indices by the altitudinal range and in general.

	Young	Middle-aged	Old	Total
Species Richness (S)	14	9	13	17
Individuals	206	115	133	454
Simpson_1-D	0.34	0.63	0.57	0.4975
Shannon_H	0.89	1.34	1.45	1.271
Margalef	2.44	1.69	2.45	2.615
Chao-1	15.00	9.50	13.00	17.33

Thus, the 454 individuals were distributed among 17 species, of which 6 are native and 11 are exotic or introduced individuals. The species with the highest abundance were Musa sp (316 individuals in total), Cordia alliodora (55 individuals in total), and Inga spp (16 individuals) while Spondias purpurea and Citrus aurantifolia are the least abundant with only 1 individual recorded in the whole study area.

The IVI reveals that in the three age ranges of the AFS the two most important species are Musa sp and Cordia alliodora with a total IVI to 115.31% and 87.06% respectively (Table 3). In the young AFS plots, there are only 4 species that exceed 10% IVI. While in the middle-age AFS plots, there are up to 9 species exceeding this limit.

Table 3

Most important species (IVI>10) by plantation age and total.

	RAa (%)	RFb (%)	RDc (%)	IVId (%)
Young
Musa sp	81.07	14.29	69.85	165.20
Cordia alliodora	6.80	19.05	14.68	40.53
Lysiloma divaricatum	0.97	9.52	2.82	13.32
Calycophyllum spruceanum	1.46	9.52	0.21	11.19
Middle-aged
Cordia alliodora	25.22	22.22	83.51	130.95
Musa sp	54.78	22.22	9.39	86.40
Inga sp.	6.96	11.11	1.92	19.99
Cocus nucifera L.	2.61	11.11	1.66	15.38
Citrus sinensis	1.74	11.11	0.04	12.89
Persea Americana	4.35	5.56	0.23	10.14
Old
Musa sp	64.66	18.18	40.12	122.96
Cordia alliodora	9.02	4.55	33.72	47.28
Persea Americana	3.76	13.64	4.75	22.15
Lysiloma divaricatum	3.76	9.09	6.61	19.46
Carica papaya	3.76	9.09	0.75	13.60
Cedrela odorata	2.26	9.09	1.47	12.82
Citrus limetta	1.50	9.09	0.38	10.98
Matisia cordata	1.50	4.55	4.90	10.95
Citrus reticulata	3.76	4.55	2.37	10.67
Total
Musa sp	69.60	18.03	27.67	115.31
Cordia alliodora	12.11	14.75	60.19	87.06
Persea Americana	2.64	8.20	1.31	12.15
Inga sp.	3.52	6.56	1.89	11.97

a RA = Relative abundance.

bRF = Relative frequency.

cRD = Relative dominance.

dIVI = Importance Value Index.

Fruit and timber species such as Musa sp and Cordia alliodora are the most dominant in the evaluated plots, and all species cultivated for cocoa shade have other potential uses, whether fruit, timber, or medicinal (Table 4). In all the evaluated plots, there is a majority of species with a low density of individuals.

Table 4

Species and abundance according to the age of AFS and in a total.

And the potential products that can be exploited from them. (E = Exotic; N = Native; F = Forest; M = Medicinal; T = Timber).

Specie	Family	Young	Middle-aged	Old	Total	Nativea	Potential Productsb
Mangifera indica	Anacardiaceae	1	3	2	6	E	F
Spondias purpurea	Anacardiaceae	1	0	0	1	E	F
Annona muricata	Annonaceae	2	0	0	2	N	F, M
Cocus nucifera L.	Arecaceae	1	3	0	4	N	F
Matisia cordata	Malvaceae	0	0	2	2	N	F
Cordia alliodora	Boraginaceae	14	29	12	55	E	T
Carica papaya	Caricaceae	0	0	5	5	E	F
Inga sp.	Fabaceae	5	8	3	16	N	F
Lysiloma divaricatum	Fabaceae	2	0	5	7	N	T
Persea americana	Lauraceae	2	5	5	12	E	F
Cedrela odorata	Meliaceae	3	1	3	7	E	T
Musa sp	Musaceae	167	63	86	316	E	F
Calycophyllum spruceanum	Rubiaceae	3	0	2	5	N	T
Citrus limetta	Rutaceae	2	1	2	5	E	F
Citrus sinensis	Rutaceae	1	2	0	3	E	F
Citrus reticulata	Rutaceae	2	0	5	7	E	F
Citrus aurantifolia	Rutaceae	0	0	1	1	E	F

a It is indicated the species is native (N) or exotic (E).

b It is indicated the potential products that can be exploited from each specie (F = Forest; M = Medicinal; T = Timber).

Composition and spatial distribution of trees in cacao AFS

The analysis of variance does not show significant statistical differences between the basal area of shade trees, basal area of cocoa trees, and total basal area (p<0.005). However, it can be observed that as the cacao plantation gets older the basal area of cocoa trees increases. Total basal area under young, middle-aged and old cacao AFS was observed to be 8.23 m2 ha-1, 9.96 m2 ha-1 and 10.95 m2 ha-1 respectively. Likewise, shade trees occupied a greater average basal area (15.92 m2 ha-1) in middle-aged cocoa AFS, while less in old cocoa AFS (4.39 m2 ha-1) and young cocoa AFS reached 5.6 m2 ha-1 of basal area for shade trees (Fig 2). Similarly, the total basal area was greater in middle-aged cocoa AFS than in young or old cacao AFS. Only in middle-aged cocoa AFS was the basal area occupied by shade trees (61.51%) greater than the area occupied by cocoa trees (38.49%). In young and adult cocoa AFS, cocoa occupied a basal area of 59.48% and 71.36% respectively of the total basal area.

Fig 2

Basal area of cocoa, shade trees, in a total and basal area of cocoa and shade trees as a percentage of the total.

Means with equal letters are not statistically different (p<0.05).

Seven of the total species studied were observed to be common in all the three age categories (Table 2; Fig 3). Spondias purpurea and Annona muricata were only reported in young cacao AFS, while Matisia cordata, Carica papaya and Citrus aurantifolia were only observed in old cacao AFS. Dissimilarity indices are higher when comparing young cocoa AFS with middle-aged or old cocoa AFS than when comparing old cocoa AFS with middle-aged cocoa AFS (Fig 4).

Fig 3

Number of species per age level of cocoa AFS.

Fig 4

Species dissimilarity between cocoa plots according to age groups.

Discussion

In our study, AFS cocoa can be differentiated among three age groups based on their diversity, species abundance and predominant species. The two predominant species in the three age levels of the cocoa AFS are Musa sp and Cordia alliodora, the first cultivated mainly for its highly marketable fruit and the second a timber specie with an important local market. In general, all the species reported are exploited either for the sale or consumption of their fruits or wood. Similarly, in cocoa AFS in Ivory Coast, Tondoh et al. [2] reported the predominance of fruit tree species in AFS and indicated that farmers planted fruit trees to provide shade and income.

The diversity reported in our study is in line with that reported in other latitudes for cacao AFS. In Central America and Mexico, Shannon’s diversity index (H´) and species richness (S) ranged from 0.8–2.99 and 22–104 [22, 23]. In the Amazon and Atlantic Forest biomes, there are AFS with variation in the number of families (11–45), S (13–180), and H´ (1.37–2.73) [24-26].

Most species found in the study have alternative uses such as food and timber. This diversification promotes the sustainability of cocoa AFS since it generates greater economic security for farmers [5, 27, 28]. This means that AFS generates social and environmental benefits without affecting the economic aspect of agricultural production [29-31]. Further, the cultivation of cocoa in AFS improves the conservation of floral diversity and management practices [23].

This trend toward the dominance of fruit, timber, and medicinal trees could be a strong indication of the deliberate transformation of the landscape by farmers from natural pioneer species that have traditionally been grown with cocoa to species that provide food and medicinal benefits [4]. Furthermore, considering that the agroecosystems evaluated in our study are spaces with a high level of anthropization, it explains the relatively low levels of diversity and the predominance of species that in addition to shade provide other benefits to the producer like wood and fruit harvest and traditional uses as medicinal trees.

Likewise, well-planned shade trees influences positive impact on cacao yield, improves net income together with various ecosystem services subject to implementation of proper management strategies [6, 32–35]. In addition, diversifying the agroecosystem with shade trees improves overall agroecosystem performance as each of these species fulfill one or more essential functions in nutrient cycling [36, 37], pest and disease control [32, 38], biomass production and carbon stocks [10, 37, 39–41].

Composition and spatial distribution of trees in cocoa AFS

Micro-parceling was also a common phenomenon observed in the study area because of the presence relatively small cultivable plots (0.5–2 ha). Asare et al. [42] and Asigbaase et al. [4] also observed micro-parceling in other places where cocoa is produced. In terms of basal area, although no significant differences are observed, higher values of the basal area occupied by cocoa trees are observed in middle-aged or old cocoa AFS rather than in young AFS. This is probably because, in older AFS, cocoa trees have been able to develop a greater stem thickness.

However, when comparing the average basal area of shade trees, it is observed that middle-aged cocoa AFS occupy a larger basal area despite having a lower density of total shade trees. This is probably due to the presence of many mature timber trees such as Cordia alliodora. These phenomena are also reported by Asigbaase et al. [4] when they evaluated organic and conventional cocoa AFS in Ghana.

Jaccard and Sorensen’s dissimilarity indices are above 50% when comparing the age groups with each other, evidencing moderate similarity between these groups. Other authors such as Asigbaase et al. [4] and Braga et al. [43] report high levels of dissimilarity; however, the main difference is that Asigbaase et al. [4] made comparisons between organic and conventional cocoa trees while in this study only organic cocoa trees are incorporated.

Conclusions

This study contributes to the knowledge of the composition and diversity of tree species communities in cocoa agroecosystems in the Amazonas region. Although no marked differences in diversity are observed and the dominance of two species used as shade is evident, it contributes to the understanding of how cocoa farmers modify and diversify the PBS.

The high levels of similarity observed are combined with the preference of cocoa farmers to grow timber or fruit tree species alongside cocoa, mostly native, diversifying their plots and obtaining economic and consumption benefits in addition to cocoa farming. This diversification, however, should be managed to improve the distribution of shade trees and improve diversification management practices that are beneficial to farmers and the environment.

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Reviewer #1: Yes

**********

4. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: No

**********

5. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: The manuscript at present form requires major modification in texts and Result presentation in tabular and or graphical form. Here are the comments that I find should be considered to increase the manuscript to a technically sound work:

1. Why there are two ‘native’ in title of the manuscript? Fine aroma is native or the Cacao is or both?

2. L13–15: Give a suitable research gap before pointing the objectives. The use of adverb in the sentence showed you have explained the research gap. However, ‘Cacao cultivation ..... species in the region’ could not speak the gaps in the knowledge base.

3. L17–18: use the value or value range within parenthesis for moderately low.

4. L20: put value/ value range for similarity within parentheses.

5. L20–22: Please rephrase this portion. It is not understandable that whether you are suggesting further diversification or concluding with present diversified systems at the first half of the sentence.

6. L23: While rephrasing, place this sentence separately before concluding statement such that it can leave a remark for conclusion. At the present form it showed an interpretation of result.

7. L24: I suggest instead of dissimilarity indices, you can use species dissimilarity. Why is ‘especies frutales’ mentioned in the keywords? I could not find same and similar word(s) anywhere in the whole manuscript except in the keywords.

8. L28–30: Whether cacao is the primary crop for which forests were partially cleared or it was for some other cultivations? Give a clearer statement in support of it.

9. L36: Give an appropriate reference to the term ‘conventional cacao system.’

10. L38: How all of a sudden it became a productive system? As just now you termed it to be simplified system requiring agrochemical dependency, which again was not properly managed by smallholders due to high input costs.

11. L39–43: This is good but, statement made- “this tendency towards ..... high input costs” and in this section are discrete.

12. L32–34: Is it reasonable to use the term agroforest/ agroforestry for Cacao system? Because, the system undergoes intense modification in respect to economic priority of the cultivars. Whereas, any agroforest should mimic the tree composition with the native forest or secondary forest. I think ‘Conventional Cacao System’ or ‘Conventional Cacao Agro-ecosystem’ would be more appropriate.

13. L56–57: Add more recent reference on expected global market demand and price hike on Cacao.

14. L63: Add specified objectives of the study.

15. L74–75: On what basis you are terming them as young, middle age, etc. Also elaborate why <8 years cacao cultivation was deselected?

16. L76: If it is 15×1.5 ha then result is 22.5 not 22.2.

17. It looks that your qudrats (sampling plots) covered an area of 1.5 ha and not 22.2/22.5 ha. Clearly state what was the total area under laid plot not the area that was covered under cultivation? Because, your sampling time i.e., November and December raised questions in covering so much big area under quadrat laying. The section ‘In the afore mentioned ... 22.2 ha sampled’ and ‘Data collection was ... sub-plot was recorded needed rigorous modification to make it clearer to the audience.

18. L84–85: Farmers are mostly aware of vernacular names not scientific name and hence modify the sentence as an appropriately.

19. L89: Give official identification address of ‘KUELAP-UNTRM’ within the parenthesis.

20. L91–92: If you write this way then give the division factor which was used in conversion of CBH to DBH.

21. L93: ‘Procesamiento y análisis de datos’ Change it to English.

22. L94–103: Give specific references to each of the analysis performed. For example for richness, for Shannon, Simpson, Margalef, Chao-1 indices, Jaccard and Sorenson.

23. L112: ‘In general, when visualizing the total data...’ Rephrase this portion.

24. L119: ‘Species richness ranged from 1-9 in the plots.’ Table 2 showed Species richness at different aged stands ranged between 9 and 17.

25. L119–120: Modify to – ‘Species richness was the lowest at middle aged (16–29 years) cacao plots.’ Are you observing only Cacao trees in the entire cultivation system? If not, then why you are mentioning middle aged cacao trees? It should be middle aged of the cultivation system.

26. L123–126: ‘Simpson's (1-D) and Shannon's .... middle-age AFS are the least diverse compared to young and old AFS.’ This should be in discussion. Cite results of the diversity indices here.

27. L128: At L121 you have mentioned that total 16 species were observed in the study area; here you are mentioning 454 individuals were distributed among 17 species distributed; and table 3 representing 17 species.

28. Table 3: Give references below table which was used to delineate the species as exotic, native etc. or add a section at method how you have distinguished this?

29. Table 3: What is potential products? Add a section in the manuscript how it was enumerated and how important it is in phytosociological studies?

30. L137–144: ‘The IVI reveals that .... with a low density of individuals.’ This is not proper result writing. You should give the Dr, Fr, Dor, IVI, etc. values representing the valuable species. This section is neither complete result nor complete discussion.

31. How you have calculated IVI? Add a section in the method. Because it looks absolute value, and you are giving percent symbol. Better to use RIVI, this will give more clear expression of observed species.

32. Figure 2: What are Joven, Madura and Adulta? If these are vernacular then give explanation of the term in figure caption.

33. L153–154: ‘there was a total of 8.23 m*ha2-1, 9.96 ..... and old cocoa AFS respectively.’ Should be written as- ‘Total basal area under young, middle-aged and old cacao AFS was observed to be 8.23 m2 ha-1, 9.96 m2 ha-1 and 10.95 m2 ha-1 respectively.

34. ‘m*ha2-1’: Correct it to ‘m2 ha-1’ across the whole manuscript. The digit 2 should be at superscript of m expressing as squared meter and -1 should be superscripted at ha denoting per hectare.

35. L169: ‘Of the total .... in the three age rang’ change it to – ‘Seven of the total species studied were observed to be common in all the three age categories.’

36. The term ‘reported’ should be changed to observed, found, etc.

37. Figure 4: Change the language of axis title to English.

38. Shannon diversity index (H0) is not the correct expression. It should be H´.

39. L185–191: ‘The Cacao ecological zone .... looks notably promising.’ This section is not relevant for your research. I suggest change these explanations with relevant texts.

40. At the very beginning of discussion avoid citing and linking with earlier reports. Start discussion with some productive phrases relevant to your findings.

41. L200–201: A well-planned shade trees influences positive impact on cacao yield, improved net income together with various ecosystem services subject to implementation of proper management strategies (References).

42. L213: ‘Côte d'Ivoire’, change it to English, if not possible give description within parenthesis.

43. L222: that additionally provides other benefits (name some other benefits in this parenthesis) together with shade.

44. L224–225: Micro-parcelling (give brief description of micro-parcelling) was also a common phenomena observed in the study area because of the presence relatively small cultivable plots (0.5–2 ha).

45. L230–231: ‘since the density ... higher density of cacao plants.’ This explanation is not required.

46. L235¬–236: ‘which in young AFS .... so they have a lower density.’ It is a obvious fact so, this portion is not required.

47. L239–240: Jaccard’s and Sorenson’s are similarity indices. They evaluate similarity not dissimilarity. You can evaluate inverse Jaccard or inverse Sorenson for dissimilarity estimation. In such instances you have to explain how the dissimilarity or inverse similarity was evaluated in the methodology.

**********

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Reviewer #1: Yes: Panna Chandra Nath

[NOTE: If reviewer comments were submitted as an attachment file, they will be attached to this email and accessible via the submission site. Please log into your account, locate the manuscript record, and check for the action link "View Attachments". If this link does not appear, there are no attachment files.]

While revising your submission, please upload your figure files to the Preflight Analysis and Conversion Engine (PACE) digital diagnostic tool, https://pacev2.apexcovantage.com/. PACE helps ensure that figures meet PLOS requirements. To use PACE, you must first register as a user. Registration is free. Then, login and navigate to the UPLOAD tab, where you will find detailed instructions on how to use the tool. If you encounter any issues or have any questions when using PACE, please email PLOS at figures@plos.org. Please note that Supporting Information files do not need this step.

Submitted filename: PONE-D-22-03463_reviewer.docx

Click here for additional data file.

3 Aug 2022

I. Journal Requirements:

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We ensure that the manuscript meets with PLOS ONE´s requirements.

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When you resubmit, please ensure that you provide the correct grant numbers for the awards you received for your study in the ‘Funding Information’ section.

We recheck it.

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“The authors thank the Fondo Nacional de Desarrollo Científico, Tecnológico y de Innovación Tecnológica (FONDECYT) for funding this research through the Contract N° 026-2016 of the "Círculo de Investigación para la Innovación y el fortalecimiento de la cadena de valor del cacao nativo fino de aroma en la zona nor oriental del Perú-CINCACAO" project, executed by the Instituto de Investigación para el Desarrollo Sustentable de Ceja de Selva (INDES – CES), de la Universidad Nacional Toribio Rodríguez de Mendoza de Amazonas. “

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“The authors thank the Fondo Nacional de Desarrollo Científico, Tecnológico y de Innovación Tecnológica (FONDECYT) for funding this research through the Contract N° 026-2016 of the "Círculo de Investigación para la Innovación y el fortalecimiento de la cadena de valor del cacao nativo fino de aroma en la zona nor oriental del Perú-CINCACAO" project, executed by the Instituto de Investigación para el Desarrollo Sustentable de Ceja de Selva (INDES – CES), de la Universidad Nacional Toribio Rodríguez de Mendoza de Amazonas.”

We note that you have provided additional information within the Acknowledgements Section that is not currently declared in your Funding Statement. Please note that funding information should not appear in the Acknowledgments section or other areas of your manuscript. We will only publish funding information present in the Funding Statement section of the online submission form.

We delete this section.

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We provide a information about map obtaining in the figure 1 caption.

II. Review Comments to the Author

Below we described the actions that we make for response a reviewer recommendations/comment:

1. Why there are two ‘native’ in title of the manuscript? Fine aroma is native or the Cacao is or both?

There was a writing issue. It was corrected.

2. L13–15: Give a suitable research gap before pointing the objectives. The use of adverb in the sentence showed you have explained the research gap. However, ‘Cacao cultivation ..... species in the region’ could not speak the gaps in the knowledge base.

14-15: A new sentence providing a research gap was included.

3. L17–18: use the value or value range within parenthesis for moderately low.

L18: A diversity index value range was provided.

4. L20: put value/ value range for similarity within parentheses.

L21: Value was put.

5. L20–22: Please rephrase this portion. It is not understandable that whether you are suggesting further diversification or concluding with present diversified systems at the first half of the sentence.

L21-24: We were rephrasing this sentence.

6. L23: While rephrasing, place this sentence separately before concluding statement such that it can leave a remark for conclusion. At the present form it showed an interpretation of result.

Done.

7. L24: I suggest instead of dissimilarity indices, you can use species dissimilarity. Why is ‘especies frutales’ mentioned in the keywords? I could not find same and similar word(s) anywhere in the whole manuscript except in the keywords.

L25: We take the recommendation, we use species dissimilarity instead dissimilarity indices. Also, instead “species frutales” we put the translation “fruit species”

8. L28–30: Whether cacao is the primary crop for which forests were partially cleared or it was for some other cultivations? Give a clearer statement in support of it.

L30: We rephrase it

9. L36: Give an appropriate reference to the term ‘conventional cacao system.’.

L38: A reference was provided.

10. L38: How all of a sudden it became a productive system? As just now you termed it to be simplified system requiring agrochemical dependency, which again was not properly managed by smallholders due to high input costs.

We corrected it.

11. L39–43: This is good but, statement made- “this tendency towards ..... high input costs” and in this section are discrete.

L36-41: We rephrase it to better understanding.

12. L32–34: Is it reasonable to use the term agroforest/ agroforestry for Cacao system? Because, the system undergoes intense modification in respect to economic priority of the cultivars. Whereas, any agroforest should mimic the tree composition with the native forest or secondary forest. I think ‘Conventional Cacao System’ or ‘Conventional Cacao Agro-ecosystem’ would be more appropriate.

L35-39: We change the term.

13. L56–57: Add more recent reference on expected global market demand and price hike on Cacao.

L57-59: We changed the sentence and provided more recent information.

14. L63: Add specified objectives of the study.

L64-69: Specific objectives was added.

15. L74–75: On what basis you are terming them as young, middle age, etc. Also elaborate why <8 years cacao cultivation was deselected?

L:88-91: We add an explanation with reference for this selection criteria.

16. L76: If it is 15×1.5 ha then result is 22.5 not 22.2.

L95: We corrected this in all document.

17. It looks that your qudrats (sampling plots) covered an area of 1.5 ha and not 22.2/22.5 ha. Clearly state what was the total area under laid plot not the area that was covered under cultivation? Because, your sampling time i.e., November and December raised questions in covering so much big area under quadrat laying. The section ‘In the afore mentioned ... 22.2 ha sampled’ and ‘Data collection was ... sub-plot was recorded needed rigorous modification to make it clearer to the audience.

It was rephrased to clearer for the audience.

18. L84–85: Farmers are mostly aware of vernacular names not scientific name and hence modify the sentence as an appropriately.

L97-100: We were modifying the sentence.

19. L89: Give official identification address of ‘KUELAP-UNTRM’ within the parenthesis.

L102: Address was provided.

20. L91–92: If you write this way then give the division factor which was used in conversion of CBH to DBH.

L109: The conversion factor was provided.

21. L93: ‘Procesamiento y análisis de datos’ Change it to English.

L110: Done

22. L94–103: Give specific references to each of the analysis performed. For example, for richness, for Shannon, Simpson, Margalef, Chao-1 indices, Jaccard and Sorenson.

L114: A references was provided.

23. L112: ‘In general, when visualizing the total data...’ Rephrase this portion.

L137-138: It was rephrased.

24. L119: ‘Species richness ranged from 1-9 in the plots.’ Table 2 showed Species richness at different aged stands ranged between 9 and 17.

a. L119–120: Modify to – ‘Species richness was the lowest at middle aged (16–29 years) cacao plots.’ Are you observing only Cacao trees in the entire cultivation system? If not, then why you are mentioning middle aged cacao trees? It should be middle aged of the cultivation system.

L144-149: We were rewriting this for better understanding.

25. L123–126: ‘Simpson's (1-D) and Shannon's .... middle-age AFS are the least diverse compared to young and old AFS.’ This should be in discussion. Cite results of the diversity indices here.

L147-149: This sentence was rewrite.

26. L128: At L121 you have mentioned that total 16 species were observed in the study area; here you are mentioning 454 individuals were distributed among 17 species distributed; and table 3 representing 17 species.

L151: We corrected, effectively it was 17 species.

27. Table 3: Give references below table which was used to delineate the species as exotic, native etc. or add a section at method how you have distinguished this?

L103-105: We added a section at methods (L:91-93)

28. Table 3: What is potential products? Add a section in the manuscript how it was enumerated and how important it is in phytosociological studies?

L103-105: We added a sentence explaining how we enumerate the potential products.

29. L137–144: ‘The IVI reveals that .... with a low density of individuals.’ This is not proper result writing. You should give the Dr, Fr, Dor, IVI, etc. values representing the valuable species. This section is neither complete result nor complete discussion.

L59: we rewrite and added IVI values for the most important species to improve this sentence.

30. How you have calculated IVI? Add a section in the method. Because it looks absolute value, and you are giving percent symbol. Better to use RIVI, this will give more clear expression of observed species.

L117-122: We added a section in “materials and methods” to explain how IVI was calculated.

31. Figure 2: What are Joven, Madura and Adulta? If these are vernacular then give explanation of the term in figure caption.

We corrected the language for figure.

32. L153–154: ‘there was a total of 8.23 m*ha2-1, 9.96 ..... and old cocoa AFS respectively.’ Should be written as- ‘Total basal area under young, middle-aged and old cacao AFS was observed to be 8.23 m2 ha-1, 9.96 m2 ha-1 and 10.95 m2 ha-1 respectively.

L177-179: We take the recommendation.

33. ‘m*ha2-1’: Correct it to ‘m2 ha-1’ across the whole manuscript. The digit 2 should be at superscript of m expressing as squared meter and -1 should be superscripted at ha denoting per hectare.

Done.

34. L169: ‘Of the total .... in the three age rang’ change it to – ‘Seven of the total species studied were observed to be common in all the three age categories.’

L191: We take the recommendation

35. The term ‘reported’ should be changed to observed, found, etc.

Done

36. Figure 4: Change the language of axis title to English.

Done.

37. Shannon diversity index (H0) is not the correct expression. It should be H´.

The expression was checked in hole document.

38. L185–191: ‘The Cacao ecological zone .... looks notably promising.’ This section is not relevant for your research. I suggest change these explanations with relevant texts.

We had decided delete this paragraph.

39. At the very beginning of discussion avoid citing and linking with earlier reports. Start discussion with some productive phrases relevant to your findings.

We rephrasing and reorder this section to improve it.

40. L200–201: A well-planned shade trees influences positive impact on cacao yield, improved net income together with various ecosystem services subject to implementation of proper management strategies (References).

L231-233: We take the recommendation and made the changes.

41. L213: ‘Côte d'Ivoire’, change it to English, if not possible give description within parenthesis.

L206: Changed

42. L222: that additionally provides other benefits (name some other benefits in this parenthesis) together with shade.

L229-230: We added this other benefits

43. L224–225: Micro-parcelling (give brief description of micro-parcelling) was also a common phenomena observed in the study area because of the presence relatively small cultivable plots (0.5–2 ha).

L241-243: We take this recommendation and rewrite the sentence.

44. L230–231: ‘since the density ... higher density of cacao plants.’ This explanation is not required.

We deleted it.

45. L235¬–236: ‘which in young AFS .... so they have a lower density.’ It is a obvious fact so, this portion is not required.

We deleted it.

46. L239–240: Jaccard’s and Sorenson’s are similarity indices. They evaluate similarity not dissimilarity. You can evaluate inverse Jaccard or inverse Sorenson for dissimilarity estimation. In such instances you have to explain how the dissimilarity or inverse similarity was evaluated in the methodology.

L125: We added a reference in the “Materials and Methods section”

Submitted filename: Response to reviewers.docx

Click here for additional data file.

31 Aug 2022

8 Sep 2022

Dear editor and reviewers, We thank you all for the constructive comments provided. We believe that addressing every single one of them has improved significantly the manuscript. The response for specific comments are in the attached file labeled as "Response letter".

The authors

Submitted filename: Response Letter.docx

Click here for additional data file.

27 Sep 2022

Tree diversity in agroforestry systems of native fine-aroma cacao, Amazonas, Peru

PONE-D-22-03463R2

Dear Dr. Goñas,

We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements.

Within one week, you’ll receive an e-mail detailing the required amendments. When these have been addressed, you’ll receive a formal acceptance letter and your manuscript will be scheduled for publication.

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Kind regards,

Arun Jyoti Nath

Academic Editor

PLOS ONE

Additional Editor Comments (optional):

Reviewers' comments:

3 Oct 2022

PONE-D-22-03463R2

Tree diversity in agroforestry systems of native fine-aroma cacao, Amazonas, Peru

Dear Dr. Goñas:

I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now with our production department.

If your institution or institutions have a press office, please let them know about your upcoming paper now to help maximize its impact. If they'll be preparing press materials, please inform our press team within the next 48 hours. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information please contact onepress@plos.org.

If we can help with anything else, please email us at plosone@plos.org.

Thank you for submitting your work to PLOS ONE and supporting open access.

Kind regards,

PLOS ONE Editorial Office Staff

on behalf of

Dr. Arun Jyoti Nath

Academic Editor

PLOS ONE