Introduction

Forests provide a diversity of ecosystem goods and services at local, regional and global scales, on which many communities depend (^{Morgan et al., 2022}). Despite this, deforestation in the tropics continues inexorably with serious implications for biodiversity conservation, climate regulation and ecosystem services. Rapid expansion of the agricultural frontier, livestock and illegal logging have converted the world's last remnants of tropical forest into isolated patches, a situation that endangers the continuity of this ecosystem (^{Da Ponte et al., 2017}).

The Alto Paraná Atlantic forests (APAF) is one of the most threatened tropical forests in the world. In this regard, only 9% of the original forest cover remains in Paraguay, mostly in a highly fragmented and degraded state (^{Da Ponte et al., 2017}; ^{World Wide Fund for Nature [WWF], 2016}). As mentioned by ^{Peralta-Kulik et al. (2018}), additional forest valuation efforts are still needed in Paraguay, because of the need for information on the specific ecosystem services for each ecoregion and the economic value they could report by the best-known direct uses such as timber, fuelwood and some non-timber forest products.

Non-timber forest products (NTFP) are part of the so-called provisioning services within the categories of ecosystem services (^{Millennium Ecosystem Assessment [MEA], 2005}). In Paraguay, although considerable progress has been made in the field of forest economic value research (^{Merenciano et al., 2018}; ^{Peralta-Kulik et al., 2018}; ^{Quevedo et al., 2013}, ²⁰²¹), the evaluation of NTFPs is still a pending task, taking into account broad conservation or sustainable forest management objectives.

According to ^{Balvanera et al. (2012}), in Latin America there are notable differences in the study of ecosystem services, reflecting the specific historical context, pressures and needs of each nation. A set of conceptual and methodological approaches have been used for environmental economic valuation in the region, inspired by the research of ^{Costanza et al. (1997}). Regarding specific research on the economic valuation of NTFPs, Argentina has made progress in the estimation of the use of medicinal, food and dye plants (^{Sarmiento et al., 2020}, ²⁰²²). Other examples are the study of ^{Duchelle et al. (2012}) and ^{Frey et al. (2019}) in Brazil and the United States, respectively, although there is scarce information on this type of research (Frey et al., 2019; ^{Sarmiento et al., 2022}).

^{Small et al. (2017}) mention that the challenge of valuing non-material benefits remains. According to ^{Sarmiento et al. (2020}) it is necessary to analyze other values of ecosystem services such as biodiversity conservation, carbon sequestration or water quality in the region. Currently, the literature recognizes the need to integrate biophysical, economic and sociocultural assessments to support decision making related to integrated ecosystem management (^{Peralta-Kulik et al., 2018}; ^{Sarmiento et al., 2022}).

The objective of this research was to estimate the economic direct use value expressed by NTFP in the Alto Paraná Atlantic forests, Paraguay to complement other economic valuations of the same forest that suggest greater competitiveness of this ecosystem compared to other land uses. It is important to emphasize that this is a pioneering study at the national level and that it was carried out in a permanent biodiversity monitoring plot. The economic estimation facilitates decision making by those responsible for the management and conservation of forest ecosystems, to maintain the provision of ecosystem services in the long term, facilitate mechanisms to contribute to landscape connectivity and value the goods and services derived from the forest in a more complete manner.

Materials and Methods

Results

Discussion

The results not only provided information on the monetary value of NTFPs in the Alto Paraná Atlantic forests, but also provided relevant qualitative information for the design of conservation strategies for important forest fragments in the country.

Forest products such as fruits, wild animals, honey, medicines, fibers and fuel are part of the livelihood strategies of forest-dependent communities in Paraguay and have both livelihood and commercial value (^{Walcott et al., 2015}). Meanwhile, ^{FAO (2014)} indicates that forest food gathering is also considered important when other food sources fail.

In Paraguay, several authors report varying numbers of species, including native and introduced species used as medicinal plants, which easily exceed 300 species (^{Degen de Arrúa et al., 2019}). In this research, the medicinal category was the best represented (71 %), which supports that cited by ^{Dujak et al. (2015}) on the deep-rooted use of native plants for medicinal purposes in the Paraguayan popular culture. Medicinal plants are widely used as traditional medicine in the country, both in rural and urban communities (^{Ferro, 2019}). In a study carried out in the communities of Itá Azul and San Gervasio (Guairá Department), ^{Degen de Arrúa and González (2014)} reported 68 species of medicinal use distributed in 35 families, the most important were Asteraceae (19 %), Rutaceae (9 %) and Fabaceae, Lamiaceae and Verbenaceae (6 % each); 53 % of the reported species were native. These authors observed that these communities are not involved in the commercialization of medicinal plants, but use them for self-consumption via direct extraction from their habitat or from small domestic crops. The authors mention that ethnopharmacobotanical knowledge is passed verbally from one generation to the next, mainly by women.

On the other hand, ^{Soria and Basualdo (2015}) mention that plants marketed in Paraguay for medicinal purposes, mainly from their natural habitat, are threatened in their survival. They are also affected by the overexploitation to which they are subjected for commercial use, either locally or internationally, when they represent raw material for herbal medicines, in more industrialized processes for phytotherapeutics or various industrial processes.

As for the ornamental uses of NTFPs, due to its subtropical nature and varied habitats that respond to this type of climate, Paraguay has an important diversity of orchids. The largest orchid collections cited in the country come from the Eastern Region (^{Schinini, 2010}). ^{Rolón et al. (2002)} described 61 orchid species in the Reserva Natural del Bosque Mbaracayú, a protected area located in a transition zone between the Alto Paraná Atlantic forests and Cerrados. Among the common species in this research, we found Miltonia sp., O. maculata and Acianthera sp., all commercialized nationally for ornamental uses.

The native peoples of Paraguay selectively extract wood for the production of handicrafts for sale in the cities and have explored options for the sustainable harvesting of traditional forest resources for commercial use, such as yerba mate (Ilex paraguariensis A. St.-Hil.); however, detailed information on the financial contributions of NTFPs to the livelihoods of indigenous and other local populations is not available (^{Walcott et al., 2015}).

^{Gauto et al. (2016}) note that the uses of palms are many and highlight the practice of traditional handicrafts as a particularity of these communities, using the leaves of Syagrus romanzoffiana (Cham.) Glassman (pindó) as the main material, a species recorded in the forest of the present study.

A study by ^{Dujak et al. (2015}) determined 100 plant species linked to food in two communities (Mbyá - Guaraní) inhabiting the APAF. The species were distributed in 41 botanical families and 83 genera. At the generic level, the most representative ones correspond to Citrus and Campomanesia. These include: Campomanesia xanthocarpa O. Berg, S. romanzoffiana, Carica papaya L., Jacaratia spinosa (Aubl.) A. DC., Inga uraguensis Hook. & Arn., Maclura tinctoria (L.) Steud. ssp. tinctoria, Plinia rivularis (Cambess.) Rotman, Chloroluma gonocarpa (Mart. & Eichler) Baill. ex Aubrév. and T. bipinnatifidum, which were also recorded in this research.

The NTFPs found in this research are similar to those recorded in other studies in Latin America, showing that medicinal and ornamental uses are the best represented (^{López & Cavelier, 2007}); however, there are variations compared to other publications in the region, where food use is the second-best represented category (^{Aguirre et al., 2019}).

At the local level there are still few published experiences on ecosystem services valuation (^{Merenciano et al., 2018}); for example, in the Humid Chaco ecoregion the economic value of direct use of goods (standing timber with 20 timber species) was estimated at 2 586 850 PYG∙ha^-1 or 476 USD∙ha^-1 (Merenciano et al., 2018). Another forest valuation effort in Paraguay is that of ^{Peralta-Kulik et al. (2018}) in the Alto Paraná ecoregion (APAF), where the economic values of direct (standing timber with 16 timber species) and indirect (carbon stored with 414 t CO₂e∙ha^-1), at 4 269 622 PYG∙ha^-1 or 785 USD∙ha^-1 and 652 528 PYG∙ha^-1 or 120 USD∙ha^-1, respectively. These amounts are values below those found in this research. These differences demonstrate the importance of considering NTFPs in sustainable management or other forest ecosystem conservation actions. According to ^{Costanza et al. (2017}) it is common that trees for timber are quantified and valued, but the services of climate regulation, flood control, and recreational opportunities are not considered. As a result, the contribution of such services to human well-being is ignored in policy decision making. Therefore, environmental economic valuation aims to demonstrate that functioning, intact and standing ecosystems produce valuable services that often outweigh the results of their extraction and exploitation.

Regarding the economic value of NTFPs in the region, some experiences can be reported in rural areas in the province of Santiago del Estero, Argentina, using the contingent valuation method, where the values were 61 USD∙year^-1 for medicinal uses, 1 602 USD∙year^-1 for dye species and 1 237 USD∙year^-1 for food plants (^{Sarmiento et al., 2020}). The results expressed in monetary terms demonstrate the importance of the services that native forests provide to local communities.

Variations between the present estimate and the economic values of the forest reported in other studies were possibly due to the use of different valuation methods, different ecoregions and the inclusion of non-timber products, which, in turn, differ according to the categories of uses considered. Furthermore, as mentioned by ^{Luswaga and Nuppenau (2020}), the flow of benefits depends on the conservation condition of the forest, which is a result of management and may vary between approaches.

Paraguay has a tradition in the use and consumption of NTFPs (^{Walcott et al., 2015}); however, their real value and potential are not known, a situation that is reflected in the limited qualitative and quantitative information. Even in other Latin American countries it is mentioned that studies of NTFPs, in economic terms, are scarce (^{Anastacio-Martínez et al., 2016}).

The use of natural resource assessments to inform decision makers is limited and most studies are qualitative in nature (^{Schaafsma et al., 2014}). These are generally quite localized; that is, they focus on one forest or community and the results do not incorporate the heterogeneity of ecosystem services. According to Schaafsma et al. (2014), these gaps induce the risk that NTFP values are completely omitted from strategic decision-making processes if site-specific information is not available, leading to potentially severe effects on local welfare in forest-dependent areas. According to ^{Daily et al. (2009}), there is a growing need at the national and international policy level for projections at large spatial scales of the economic values that local communities extract from forests, including that of NTFPs.

Ecosystem services and their valuation are a tool to contribute to the sustainable well-being of humanity (^{Costanza et al., 2017}). Furthermore, in cases where the value of NTFPs is recognized, there is a relevant potential incentive to maintain standing forests. It is therefore necessary to consider the integrity of forest ecosystems and recognize the multiple ecosystem services that should be incorporated into economic estimates (^{Morgan et al., 2022}), including non-timber products. In this context, it should be considered that the advantages of the methodology suggested in this research are the simplicity to evaluate NTFPs individually, the limited number of data required and the simplicity of the method to be reproduced in other ecoregions. Meanwhile, the main limitation typical of economic valuations based on market price methods which, as argued by ^{Turner et al. (2016}), is that they only work for ecosystem services that are traded in the market (mainly provisioning services). It should also be mentioned that the approximate amounts in this research correspond to partial values, since non-tree species determined at family level or with different uses were not considered; however, it is a useful tool to have an approximation of the values of the forest via its NTFPs, which traditionally have not been included in the economic valuation.

Finally, it should be mentioned that while exclusively economic approaches can to some extent interpret ecosystem services in publicly understandable metrics, they also hinder the description of cultural components (^{Loc et al., 2018}). As ^{Kenter et al. (2015}) indicate, a combination of monetary and non-monetary valuation processes and deliberative assessment processes are required for the generation of sustainable ecosystem options to be possible.

Conclusions

The economic value of direct use expressed by non-timber forest products (NTFPs) of the Alto Paraná Atlantic forests, Paraguay, was estimated at 2 270 USD∙ha^-1 for seven ornamental species with a market price (Thaumatophyllum bipinnatifidum, Billbergia nutans, Didymochlaena truncatula, Miltonia sp., Oeceoclades maculata, Acianthera sp. and Chusquea ramosissima Lindm.). This reference amount represents the important role of non-timber products in the sustainable management of tropical forests. Therefore, it reaffirms the need for additional forest valuation efforts in Paraguay that include NTFPs and other ecosystem services not yet addressed, using similar methodologies to generate useful information for decision makers on a comparable level, taking into account the information gaps at the country level for each ecoregion.