Management of Pindo Palm (Syagrus Romanzoffiana Arecaceae) in Rearing of Coleoptera Edible Larvae by the Guarani of Northeastern

RESEARCH ARTICLE

Ethnobiology and Conservation 2018, 7:01 (5 December 2017) doi:10.15451/ec2018­01­7.01­1­18 ISSN 2238­4782 ethnobioconservation.com Management of pindo palm (Syagrus romanzoffiana Arecaceae) in rearing of Coleoptera edible larvae by the Guarani of Northeastern Argentina Jorge Justino Araujo1, 2, Héctor Alejandro Keller2, 3, Norma Inés Hilgert1, 2*

ABSTRACT

Rearing of coleopteran larvae on palm tree stems as a food source is extended among Amerindian groups is as a food source as coleopteran larvae are reared on their stems. Guarani groups settled in the province of Misiones, in northeastern Argentina, consume three species of Dryophthoridae larvae (Metamasius hemipterus, Rhynchophorus palmarum and Rhinostomus barbirostris) which are rear in the stipes of Syagrus romanzoffiana palm. This work deals with the management of the different stages of growth of this palm to promote the development of the three edible larvae species. Field observation suggests a great knowledge of these insects ecology and of the differential characteristics of the palm tree wood anatomical structure throughout its ontogenic development. This constitutes the first record of the use of Metamasius hemipterus as food for the Mbya Guarani people.

Keywords: Atlantic Forest; Edible Insects; Metamasius hemipterus; Rhinostomus barbirostris; Rhynchophorus palmarum; Ethnoentomology.

1 Instituto de Biología Subtropical, IBS­CONICET. Universidad Nacional de Misiones. Bertoni 85, (3370) Puerto Iguazú, Misiones, Argentina

2 Facultad de Ciencias Forestales, Universidad Nacional de Misiones

3 Instituto de Botánica del Nordeste, UNNE­CONICET. Sargento Cabral 2131, C.C.:209, (3400) Corrientes, Argentina

* Corresponding author. E­mail address: JJA ([email protected]), HAK ([email protected]), NIH ([email protected])

INTRODUCTION Ethnoentomology (Posey 1987). The consumption of edible insects has Insects occupy an important space in the been documented since the Paleolithic socio­economic development of peoples (Hernández­Pacheco 1921). This habit is (Costa Neto 2004). The study of insects as present all over the planet and sometimes food, as well as the knowledge and species of the same genus are used and management associated with this use are raised similarly in all continents (Ramos­ part of the main objectives of Elorduy et al. 2009). Based on the empirical

1 Araujo et al 2018. Management of pindo palm (Syagrus romanzoffiana, Arecaceae) in rearing of Coleoptera edible larvae by the Guarani of Northeastern Argentina Ethnobio Conserv 6:20

knowledge of rural populations there is a Zambrana et al. 2016). Most of these record of about 1,800 edible species used by contributions on the use and management of more than 3,000 ethnic groups (Ramos­ palm trees come from the Amazon Elorduy 1997). Occasionally the rearing of rainforest. edible larvae is promoted in different plant The genus Syagrus currently comprises species (Cebolla Badie 2009; Coimbra 1984; 65 species, 2 subspecies and 14 natural Keller 2010; Mitsuhashi 2017). This practice hybrids; it is distributed in the Neotropic, by indigenous groups has been named being S. romanzoffiana (Cham.) Glassman "cultivation" (Choo et al. 2009; Dufour 1987) the species with the southernmost or "semi­cultivation" in several papers distribution (Noblick 2017). In fact, the (Cebolla Badie 2009; Defoliart 1995; Van natural distribution of this species includes Itterbeeck and Van Huis, 2012) while others eastern and southern central Brazil, eastern call it “breeding” (Cerda et al. 1999). In some Paraguay, eastern Uruguay and tropical regions this activity has reached northeastern Argentina, where it is present in commercial importance, where larvae are the province of Misiones, Corrientes, Entre sold in popular markets and in luxurious Ríos, Buenos Aires, Chaco, Santa Fe and restaurants (Delgado et al. 2008; Formosa (Cabral and Castro 2007). Hanboonsong et al. 2013; Paniagua­ Common uses of S. romanzoffiana Zambrana et al. 2014). documented for different indigenous groups Arecaceae is one the most frequently of the Atlantic Forest are food, construction, used botanical families for larval rearing. textiles, medicine and religion (Bonomo and This family is of economic, material and Capeletti 2014; Cárdenas 1989; Dawson spiritual importance in the daily life of and Gancedo 1977; Hurrell et al. 2010; millions of people, providing beverages, Keller 2014; Pochettino 2015; Reitz 1974; food, drugs, households, clothing, fuel and Rosso and Scarpa 2012). This palm fibers (Dransfield et al. 2008). It includes 200 provides a great variety of material and is of genera and 2450 species which are symbolic use to Guarani people in the distributed in the tropical and subtropical province of Misiones, at least 78 different areas of both hemispheres (Borchsenius and applications have been documented in an Moraes 2006). There are numerous studies ethnobotanical study (Keller 2008). about their relationship with human In the region of this study, the rearing of populations: i.e. a review of useful palms edible larvae of Coleoptera grown on S. around the world (Balick and Beck 1990); romanzoffiana palm stipes and other tree their ethnobotany in the Neotropics (Balick species was reported first by Ambrosetti 1984); the management of different genera (1894) and then by Martínez Crovetto in South America (Balslev 2011; Bernal et al. (1968), who recorded the development of 2011). In South America, a wide variety of edible larvae of the curculionid beetle applications are mentioned for the Rhynchophorus palmarum L. These authors Arecaceae family including: food, medicine, mention that this beetle grubs are also called veterinary, cultural, environmental, toxic, tambú by the indigenous people. In others fuel, among others (e.g. Baslev 2011; Baslev studies there has been registered pumpkins, et al. 2015; Bernal and Galeano 2013; mud vessels, hollow logs, palm spathe and Bernal et al. 2011; Blacutt­Rivero et al. 2016; hollow reeds as traditional elements used to Gragson 1992; Macia et al. 2011; Paniagua­ transport larvae from the forest to domestic

2 Araujo et al 2018. Management of pindo palm (Syagrus romanzoffiana, Arecaceae) in rearing of Coleoptera edible larvae by the Guarani of Northeastern Argentina Ethnobio Conserv 6:20

environments (Cebolla Badie 2009; Keller Paranaense a semi­deciduous forest (Placci 2008; Mayntzhusen; 2009; Müller 1989). and Di Bitetti 2006) placed in a subtropical According to the most recent climate with maximum temperatures around ethnobiological research (Cebolla Badie 40°C and minimum temperatures reaching 2009, Keller 2008) these traditional practices the point of frost and with almost continue until the present in Guarani homogeneous rains throughout the year settlements located in the Green Corridor (Crespo 1982). and the Yabotí Biosphere Reserve, in Archeological evidence of lytic industry Misiones Province. In these studies, confirms Guarani presence in Argentina as Rhynchophorus palmarum larvae rearing early as 900­2000 years BP (Noelli 2004; has been documented by the above Schmitz 1991). At present this people mentioned authors and Rhinostomus represent one of the most numerous original barbirostris (Fabricius) was registered by communities in the lowlands of South Cebolla Badie (2009). America (Assis and Garlet 2004). The management of palm trees in rural The current inhabitants of Guarani origin communities, associated with the rearing of in the province of Misiones are descendants edible larvae of Coleoptera, has been dealt from original dwellers belonging to Mbya and with in studies conducted from the Ava Chiripa communities (Ambrosetti 1894, ethnobiological perspective in different Müller 1989). At the end of the first decade regions, i.e. in Africa (Dounias 2003; Van of the XXI century their population in the Huis 2003), in Asia (Ellen 2006; province reached 13,006 inhabitants, Hanboonsong et al. 2013; Mercer 1997; distributed in approximately 100 villages Ponzetta and Paoletti 1997; Townsend (INDEC 2015). 1974), in South America (Cerda 2001; Choo In Misiones, some communities are et al. 2009; Dufour 1987; Onore 1997). settled in rural or near urban areas In the same way, unlike extractivist distributed in forest remnants along the main practices, the management of a resource roads crossing the region (Crivos et al. 2005; implies a deeper diachronic knowledge of Keller and Prance 2008). Most Guarani the components involved in the productive settlements maintain much of their traditional process, especially of the ontogenic phases subsistence of swidden agriculture, foraging, of the handled species. In this sense, the hunting and occasionally wage labor objective of this work is to provide (Felipim 2001; Jacobsen 2003). In particular, information related to the use of S. they breed beetles larvae which are romanzoffiana palms for the rearing of larvae developed in downed stipes of palm trees of three species of Dryophthoridae among and other tree species (Keller and Prance the Guarani of Northeastern Argentina. 2008). Special emphasis will be made on We conducted our study in the Mbya management practices at different stages of Guarani communities of Y aka pora, Ita piru, the palm growth. Jejy, and Chafariz (Figure 1), all located in the Guarani Department, Misiones, Study area Argentina. The Y aka pora community (26°55ˈ37" S; 54°14ˈ58" W) is located about Misiones is part of the Atlantic Forest of 6 kilometers from provincial route N° 15, it is Alto Paraná ecoregion, also known as Selva composed by six families and each family is

3 Araujo et al 2018. Management of pindo palm (Syagrus romanzoffiana, Arecaceae) in rearing of Coleoptera edible larvae by the Guarani of Northeastern Argentina Ethnobio Conserv 6:20

Figure 1. Four Guarani villages visited in this study, in the province of Misiones, Argentina made up of 4 to 5 members. The village of Cultural Papel Misionero, it currently holds a Ita piru (26°56ˈ24" S; 54°12ˈ45" W) is based land title for about 300 hectares. The on provincial route N°15, has eight families, Chafariz village (27°14ˈ50" S; 54°22ˈ01" W) with similar number of members per family. is located about six kilometers from These two communities are settled within provincial route N° 13 on the edge of the the Reserva de Uso Múltiple (RUMG) homonymous stream, it is constituted by 25 belonging to the Universidad Nacional de families, the village also has a land title for Misiones (UNaM) and administered by the 106 hectares. Facultad de Ciencias Forestales. The Jejy community (27°00ˈ29" S; 54° MATERIAL AND METHODS 09ˈ52" W) also sits on the edge of route N° 15, is made up of 70 families located within The information for this study was the premises of the Reserva Natural y collected during 12 short field trips

4 Araujo et al 2018. Management of pindo palm (Syagrus romanzoffiana, Arecaceae) in rearing of Coleoptera edible larvae by the Guarani of Northeastern Argentina Ethnobio Conserv 6:20

conducted between 2015 and 2017. To study palm which grows naturally in the studied the rearing of edible larvae of Coleoptera area. Herbarium samples were collected and developed in the S. romanzoffiana palm, we compared with material from the IBONE used the participant observation, herbarium. To translate the Guarani ethnobotanical walks and semi­structured expressions, Cadogan (1992) and Moliniers interviews (Albuquerque et al. 2014; Bernard and Genes (2003) dictionaries were used. 2000; Guber 2006; Malinowski 1922). Samples of adult beetles (Coleoptera: Along the participant observation JJA Dryophthoridae) were photographed, noticed in detail activities comprising from collected manually and preserved in 96% the palm cut for larval rearing to larvae ethyl alcohol. Insect identity was done by harvest, as well as, the different specialists (Dr. Lanteri Analia and Dr. Bello management of this palm tree according to Ayr). Samples were deposited in the Museo the type of insect to be promoted. Thirteen de La Plata, Facultad de Ciencias Naturales specimens of pindo harvested at different y Museo, UNLP, Argentina. ontogeic stages, according to local users’ The authors followed all the requirements criteria of differentiation were observed. and regulations needed for conducting Finally, informal visits to homes also ethnobiological fieldwork in Argentina. Oral contributed to understanding the social informed consent was obtained from each context, daily way of life and routines of each participant involved in this study. Information of the communities visited. provided by all participants was kept Ethnobotanical walks were made together confidential and was anonymously tracked with 4 local people (one at time) (3 from Ita using an identification number. The required Piru and 1 from Jejy villages) recognized by permissions for collection of reference members of their communities as experts materials were obtained from the Ministerio and leading actors in the activity. During the de Ecología of the Misiones province. No walks, the basic general aspects of larvae ethical approval was required for this study consumption were investigated and the in Argentina as no participants were topics to be discussed later in the semi­ subjected to any other treatment than structured interviews were identified. voluntary interviews. The research was Likewise, the basic lexemes (or semantic carried out following the code of ethics of the domain) used locally in relation to the American Anthropological Association and subject under study were identified. the International Society of Ethnobiology Finally, 19 semi­structured interviews Code of Ethics practices in place to promote were conducted in Spanish to adult men, the production of different species of edible heads of family, aged between 45 and 70 grubs. years. This represents about 18% of families and 22% of elderly men in these villages. RESULTS The topics treated in the interviews were: logging season, rearing insect species, time Practices of management the required for larval development in each Syagrus romanzoffiana palm to species, forms of larval consumption, and produce different edible coleopteran other uses of the palm tree. larvae The Syagrus romanzoffiana palm was identified in the field; it is the only species of It has been observed in the region that

5 Araujo et al 2018. Management of pindo palm (Syagrus romanzoffiana, Arecaceae) in rearing of Coleoptera edible larvae by the Guarani of Northeastern Argentina Ethnobio Conserv 6:20

the Guarani cut down the pindo palm larvae (Figure 2C) of the R. palmarum beetle Syagrus romanzoffiana (Cham.) Glassman, (Figure 2D) (however they also develop (Arecaceae) and handle the downed stipe to larvae of the weevil R. barbirostris in the promote the rearing of three species of basal part of the stem), its common name coleopteran larvae: Metamasius hemipterus, means red grubs and refers to the reddish Rhynchophorus palmarum and Rhinostomus coloration of the larvae oral apparatus, its barbirotris (Coleoptera: Dryophthoridae). adult insects are called aramandái (Table 1). The main management practice consists in Finally, in stage V (Figure 2­V) the pindo the selection of different stages of growth or tuja (old palm) plants are used specifically to ontogenic of the palm tree and the produce ycho chĩ (white grubs) larvae subsequent type of post­appendage (Figure 2E) of R. barbirostris weevils (Figure treatment applied to the stipe. Stage of 2F). Pindo tuja plants are specimens that growth presented are an emic classification reached reproductive maturity several years recognized by the Guarani and used to before. The name ycho chĩ, or white grubs define the different age groups of the palm assigned to the larvae of R. barbirostris trees. In this context, the Guarani recognize refers to the white color of it’s the oral five stages of growth, that comprise from apparatus. Adults of this species are called seedlings to adult­senile individuals (Figure chaviju (hairy snout), due to the presence of 2). hair on adult males the faces (Figure 2F). The two first stages are named I pindo Table 1 shows the different management oikotaramo (palm tree that begins to exist), II practices applied at each stage of growth of pindo yky (tender palm) seedlings and the palm and for each of the three species of tender plants of the palm without a visible weevils. stipe, neither of them is considered useful for Of the 13 specimens of Syagrus the production of larvae (Figure 2­I and 2­II). romanzoffiana cut down during the study As from stage III, each individual receives a campaigns, three correspond to growth different management practice according to stage III, eight to stage IV and two to stage its ontogenic stage, and is used for the V. The whole process constitutes an integral production of different species of food activity, cutting palm trees to produce certain larvae. The following are the species raised types of grubs involves harvest the heart of in each stage of the plant and the particular the palm or pindo ruã, since it is a food handling in each case. resource that can be consumed in situ or In stage of growth III the plants are lead to domestic areas, picking in many juvenile and immature and are called pindo cases also its fruits and occasionally yky guachu (pre­juvenile palm or literally extracting leaves for dwellings, or fibers for large tender palm) (Figure 2­III). These clothes. In general terms, the management specimens are used to produce ycho i or for the production of edible insect larva in the ycho tyrỹ larvae (Figure 2A) of the M. pindo palm includes the initial removal of hemipterus weevil (Figure 2B), its traditional lianas and small trees that surround the name means small or tender grubs, and its chosen palm to determine the direction of adult beetles are called tapoarã. In the next the fall towards an obstacle free area. Once stage IV (Figure 2­IV) the pindo pyau (young felled, the surface is either left intact or palm) plants are already in the reproductive wedge­shaped transverse incisions are stage, they are used to produce ycho pyta made along the stipe from the base to the

6 Araujo et al 2018. Management of pindo palm (Syagrus romanzoffiana, Arecaceae) in rearing of Coleoptera edible larvae by the Guarani of Northeastern Argentina Ethnobio Conserv 6:20

apex. The opening of these incisions of suitable larvae in size and quantity for depends on the individual stage of growth harvesting has been diagnosed, the stem and the species of larvae to be produced. In segments are opened longitudinally and this context, the tools used to handle the edible larvae are collected monthly in a palm are axes and machetes. harvesting day. To obtain the best larvae production per As for task division in this activity: 1) palm plant, it is necessary to cut it down during cutting is practiced mainly by adult and the moon phase jachy ray (new moon). young men, 2) the harvest is carried out by According to some interlocutors to obtain the individuals of both sexes. The activity is best productions by felled individual, it is described as follows: “ja a jaity pindo, ja necessary to have some rain a few days jaga jovái ychorã omboa ñamboguái, ja before the turning and during the larval mbo i pindo ruã jaru anguã ñande rope development. The most favorable time to cut jauva” (we will cut the pindo down, make down these plants is from September to cuts on both sides to produce larvae, March, spring and summer respectively. remove the heart and bring it home to eat). The felled palm is visited weekly to monitor larval development. Once the Rearing of the larvae optimum time has elapsed and the presence

Figure 2. I­V: Palm tree Syagrus romanzoffiana in its five stages of growth according to the local classification. A and B: larva and adult insect of Metamasius hemipterus beetle produced at stage III (scale­1 cm). C and D: larva and adult insect of Rhynchophorus palmarum weevil obtained in stage IV (scale­1 cm). E and F: larva and adult insect of Rhinostomus barbirostris beetle developed in stage V (scale­1 cm).

7 Araujo et al 2018. Management of pindo palm (Syagrus romanzoffiana, Arecaceae) in rearing of Coleoptera edible larvae by the Guarani of Northeastern Argentina Ethnobio Conserv 6:20

The ycho'i larva Metamasius hemipterus traditional way within the internodes of the rearing is explained in extenso, as takuapi cane, Merostachys claussenii Munro represented in Figure 3 and synthesized in (Poaceae) (Figure 3F), although the use of Table 1. Table 1 also summarizes details of plastic containers was also noticed (Table 1). the rearing of other two species Management practices applied to pindo in (Rhynchophorus palmarum and stage IV to promote rearing of Rhinostomus barbirostris). Those aspects Rhynchophorus palmarum larvae are not registered for M. hemipterus are showed in Figure 4 and explained in Table 1. described in detail as follows. Larvae of this species form cocoons with Once pre­rearing juvenile individuals of stem tissues (Figure 4 F) or, in some cases, the palm tree (phase III) are felled (Figure 2­ dig the soil and return to the stipe after a few III), transverse, wedge­shaped incisions are days (Figure 4 G). The Guarani call this made along the stipe (Figure 3A­B) in order phenomenon ycho o'o yvyguy (larvae move to promote ovoposition of Metamasius under the ground). hemipterus. Adult beetles of this species Management practices applied to pindo in deposit their eggs on exposed tissues in the stage V to promote rearing of ycho chĩ larva incisions (Figure 3C). For this category we Rhinostomus barbirostris larvae are showed recorded the average number of wedge­ in Figure 5 and detailed in Table 1. shaped incisions made on the stem (3). Regarding periodic diagnosis, the individuals DISCUSSION felled are visited weekly and the presence of developing larvae is evaluated. To do this, In this work the management of different the stem is gently tapped with the back side stages of growth of pindo was found to of the machete and an acoustic assessment promote the development of three species of is made according to the sound the grubs edible beetles. The Guarani of the Atlantic emit in response to the disturbance. The Forest of Argentina decide and control which sound emitted by the larvae inside the stipe species of the weevil larva to produce. For is called ycho oñe endu (larval noise). After this purpose, they select individuals of S. a certain time, two months approximately, romanzoffiana palms in different ontogenic the larvae are collected ready for stages. The results highlight a deep consumption (Figure 3D). understanding of the auto­ecology of the Larvae collection is done only once insect species; it also suggests a thorough because this species grubs develop in a knowledge of the characteristics of wood homogeneous way along the palm stipe. It is morphology along the development of this carried out from the crown to the base of the plant species. stem in all cases, the presence of larvae In relation to the classification used by the developed in the stump of the felled plant Guarani to characterize the stage of growth was also found. When these larvae reach of each individual –sensu Gatsuk et al. the pupal stage they form cocoons with palm 1980­, we found similarities with studies tissue until they become adult insects. analyzing the population structure of Guarani call the cocoon ycho raity, meaning different palm species (Souza et al. 2000, (larva nest) (Figure 3E). It has been 2003; Svenning 2002; Souza and Martins observed that transport of larvae to the 2005), as well as in the characterization of domestic environment is carried out in a the species (Bernacci et al. 2008).

8 Araujo et al 2018. Management of pindo palm (Syagrus romanzoffiana, Arecaceae) in rearing of Coleoptera edible larvae by the Guarani of Northeastern Argentina Ethnobio Conserv 6:20

Figure 3. A: Schematic of a felled pindo yky guachu palm tree with three transverse incisions along the stem. B: two specimens of felled pindo yky guachu. C: detail of wedge­shaped incisions made in the stipe. D: collected ycho'i larvae. E: Metamasius hemipterus pupa and cocoon. F: Merostachys claussenii bamboo stem used to transport larvae.

9 Araujo et al 2018. Management of pindo palm (Syagrus romanzoffiana, Arecaceae) in rearing of Coleoptera edible larvae by the Guarani of Northeastern Argentina Ethnobio Conserv 6:20

Figure 4. A: Schematic diagram of a pindo pyau palm cut downed with incisions made from the stem middle to its apex. B: Guarani cutting the palm. C: stem incisions. D: heart of the harvested palm. E: harvested ycho pyta larvae Rhynchophorus palmarum. F: larva in cocoon. G: larva inside the soil.

10 Araujo et al 2018. Management of pindo palm (Syagrus romanzoffiana, Arecaceae) in rearing of Coleoptera edible larvae by the Guarani of Northeastern Argentina Ethnobio Conserv 6:20

Figure 5. A: Schematic of a felled pindo tuja palm without incisions in the stem. B: a felled specimen pindo tuja. C: presence of sawdust on the stipe cortex. D. collection of ycho chĩ larvae and container used for transport. E: harvested ycho chĩ and ycho pyta larvae. F: Rhinostomus barbirostris larva, pupa and adult (left to right).

11 Araujo et al 2018. Management of pindo palm (Syagrus romanzoffiana, Arecaceae) in rearing of Coleoptera edible larvae by the Guarani of Northeastern Argentina Ethnobio Conserv 6:20

Table 1. Management of the palm tree S. romanzoffiana to produce three species of edible larvae of Coleoptera.

A similar management to that observed in 1973). In southern Thailand larvae is also our region for the same palm species has bred in sagu palms for commercial been cited in the Amazon for the Tatuyo purposes, maintaining the traditional method Indians (Dufour 1987) and in Paraguay of rearing in the cut plant and artificially, among the Ache Guayaqui (Clastres 1972; where the rearing is in plastic containers, Dawson and Gancedo 1977 Hill et al. 1985; using the natural substrate (Hanboonsong et Hurtado 1985), in both cases the initial use al. 2013). In Cameroon, the use of oil and of the heart, fruits and/or leaves is raffia palm (Elaeis guineensis Jacq. and mentioned. The practice of making incisions Rhapia sp. Beauv.), respectively was in the stipe with the use of old stone axes, recorded for the same purpose; in both nowadays replaced by metal ones, cases the production is for commercial (Mayntzhusen 2009; Townsend 1973) has purposes in local markets and according to also been mentioned. Dounias (2003) each expert has its specific Similar management of other palm harvesting tools and techniques. species was recorded in other regions. For We registered that palm trees are cut example, in communities’ native to New down in spring and summer which agrees Guinea, larval rearing of weevils is with that observed by Dawson and Gancedo considered a by­product of the sagu (1977) who describe that the best time for (Metroxylon sagu Rottb. and M. rumphii this activity is during the heyday of the Mart.), species that unlike S. romanzoffiana, flowering of certain species. In the same are multicaules (Ellen 2006; Mercer 1997; sense, Cadogan (1992) points out the Ponzetta and Paoletti 1997; Townsend beginning of the lapacho flowering,

12 Araujo et al 2018. Management of pindo palm (Syagrus romanzoffiana, Arecaceae) in rearing of Coleoptera edible larvae by the Guarani of Northeastern Argentina Ethnobio Conserv 6:20

Handroanthus heptaphylus (Vell.) Mattos edible larvae from their weevils and that (Bignoniaceae) "tajy potýpy pytarã jaity" (“we adult insects lay their eggs on exposed must cut down during the lapacho flowering”) tissues. Previous studies have shown that as the moment in which palm trees are felled these palm weevils require host plants with or rearing larvae of Rhynchophorus soft or damaged tissues for oviposition palmarum; and refers similarly to the (Giblin­Davis et al. 1994, 1996). It is also flowering of guavira, Campomanesia reported that male weevils of these insects xanthocarpa (Mart.) O.Berg. (Myrtaceae) for are attracted by the odor generated by palm the rearing of Rhinostomus barbirostris “chĩ tissues fermentation (Morin et al. 1986; aviju ombo a anguã guavira potýpy reity Moura et al. 1990, 1991) and that the va erã guapytangy” (to produce larvae of fermentation of the decomposing material the hairy snout it is necessary to cut down shows its maximum efficiency in 2­3 weeks palm trees when the guavira blooms). (Oehlschlager et al. 1993a, b, 2002). In According to research carried out by addition to the material from the fermented (Cebolla Badie 2013), in the past at times of plant, these insects emit an aggregation of shortage of resources (which coincides with pheromones to attract individuals of both the flowering of these two tree species), sexes (Giblin­Davis et al. 1996; Rochat et al. entire communities moved to the palm 1991; Oehlschlager 2016). In this way, the groves to use the pindo (including the local observed management suggests a production of weevil larvae) and then deep knowledge of these insects ecology returned to their homes at the time of and of the interactions with the substrates harvesting other crops. where they oviposited which contributes to The management of the different stages explain how larvae of the two desired of growth of the pindo observed in our species (M. hemipterus and R. palmarum) studied region and the development of are oriented (or attracted) by making different insect species is similar to that incisions in the palm stipes. described by Choo et al. (2009) for the Jotï With regard to the monitoring of the in Amazonas who manage the palm tree development of R. palmarum larvae in the Oenocarpus bacaba Mart. to breed larvae of palm, the use of sound emitted by the larvae Rhynchophorus palmarum and Rhinostomus as a verification system to determine the barbirostris. Nevertheless, for the production degree of occupation of these insects, of Rhynchophorus palmarum in pindo palms agrees with data recorded in the literature in our region, adult individuals in their (Coimbra 1984; Muafor et al. 2014; Van Huis reproductive stages are selected. Another 2003). Similarly, the estimation of the degree difference is that, in the case of Metamasius of infestation of R. barbirostris from the hemipterus only one harvest is made, while presence of sawdust on the stipe cortex has that of Rhinostomus barbirostris is made in been observed in other ethnicities (Choo et two stages and that of Rhynchophorus al. 2009; Dufour 1987). palmarum in three or four. The collection of larvae in two or more It was observed that Guarani from the stages (depending on the species of insect Argentinean Northeast make wedge­shaped and the ontogenetic stage of the palm tree) incisions in the downed stipe to carry out the could be based on the anatomical rearing of edible larvae of M. hemipterus and differences of the palm tissue structure (axial R. palmarum beetles and thus produce and radial) described for this botanical family

13 Araujo et al 2018. Management of pindo palm (Syagrus romanzoffiana, Arecaceae) in rearing of Coleoptera edible larvae by the Guarani of Northeastern Argentina Ethnobio Conserv 6:20

by Thomas and Franceschi (2013). identifying the adult weevil of M. hemipterus. On the other hand, in relation to the To Drs. Ma. Lelia Pochettino and Monika rearing of Rhinostomus barbirostris, the Kujawska for reviewing the manuscript and development of larvae in the senile stages of for their valuable recommendations. This the palms could be due to a strategy of the project was carried out with JJA doctoral species to avoid competition with other fellowship from CONICET. insects (Messina and Renwick 1985; Renwick 1989; Choo et al. 2009.According REFERENCES to the descriptions made by (Vaurie 1970), R. barbirostris larvae are usually attacked by Albuquerque UP, Cunha LVFC, Lucena RFP, Alves RRN (2014) Methods and Techniques in R. palmarum larvae, possibly explaining the Ethnobiology and Ethnoecology. Springer New development of both species in different York, New York, USA. portions of the stipe. Ambrosetti JB (1894) Los indios Cainguá del Alto Paraná. Boletín del Instituto Geográfico CONCLUSION Argentino 15: 661­744. Assis VD and Garlet IJ (2004) Análise sobre as The results show that the rearing of populações guarani contemporâneas: demografia, espacialidade e questões edible larvae of the three species of fundiárias. Revista de Indias 64: 35­54. Coleoptera reported here (M. hemipterus, R. Balick MJ (1984) Ethnobotany of Palms in the palmarum and R. barbirostris), is not a mere Neotropics. Advances in Economic Botany 1: 9­ act of gathering. On the contrary, it 23. represents an activity planned months in Balick MJ and Beck H (1990) Useful palms of advance, taking into account several factors, world: a synoptic bibliography. Nueva York: the stage of growth of the palm tree, the Columbia University. seasonal cycle, the lunar phase, diagnostic Balslev H (2011) Palm Harvest Impacts in elements of the forest and techniques of North­Western South America. The Botanical Review 77: 370–380. manipulation of the vegetal resource to promote the development of the desired Balslev H, Macía MJ, Navarrete H (2015) Cosecha de palmas en el noroeste de larvae. This set of activities is interpreted as Suramérica: Bases científicas para su manejo reflecting a holistic understanding by y conservación. Quito: Pontificia Universidad Guarani of the relationship between the host Católica del Ecuador. plant, insects and the biota and environment. Bernacci LC, Martins FR, Maës dos Santos FA (2008) Estrutura de estádios ontogenéticos ACKNOWLEDGEMENTS em população nativa da palmeira Syagrus romanzoffiana (Cham.) Glassman (Arecaceae). Acta Botánica Brasilera 22: 119­ To the members of the Guarani 130. communities visited for the information Bernal R, Galeano G (2013) Cosechar sin provided, to Dra. Analía Lanteri of the destruir­Aprovechamiento sostenible de Scientific Department of Entomology, Museo palmas colombianas. Facultad de Ciencias­ de la Plata, Facultad de Ciencias Naturales Instituto de Ciencias Naturales. Universidad Nacional de Colombia, Bogotá. y Museo, UNLP, Argentina for the Bernal R, Torres C, García N, Isaza C, Navarro J, identification of the species of insects R. Vallejo MI, Galeano G, Balslev H (2011) Palm palmarum and R. barbirostris, to Dr. Bello Management in South America. The Botanical Ayr, from Rio de Janeiro, Brazil for Review 77: 607­646.

14 Araujo et al 2018. Management of pindo palm (Syagrus romanzoffiana, Arecaceae) in rearing of Coleoptera edible larvae by the Guarani of Northeastern Argentina Ethnobio Conserv 6:20

Bernad HR (2000) Social Research Methods Choo J, Zent EL, Simpson BB (2009) The Qualitative and Quantitative Approaches. importance of traditional ecological Sage, University of Florida. knowledge for palm­weevil cultivation in the Blacutt­Rivero E, Moraes M, Gruca M, Balslev H Venezuelan Amazon. Journal of Ethnobiology (2016) Local knowledge about palms 29: 113–128. (Arecaceae) among children in Bolivia. Botanical Clastres P (1972) The Guayaki. In: Bicchieri MG Journal of the Linnean Society 182: 505­516. (ed) Hunters and gatherers today. Holt, Rhinehart Bonomo M, Capeletti LE (2014) Uso and Winston, New York, pp. 38­74. prehispánico de las palmeras Syagrus Coimbra CEA, (1984) Estudos de ecologia romanzoffiana y Butia yatay en el Nordeste humana entre os Suruĩ do parque indígena argentino: aportes desde la etnografía y la Aripuanã, Rondõnia. 1. O uso de larvas de biometría. Revista del Museo de Antropología coleópteros (Bruchidae e Curculionidae) na 7(2): 227­234. alimentação. Revista Brasileira de Zoología, Borchsenius F, Moraes MR (2006) Palmeras 2(2): 35­47. andinas. In: Moraes RM, Øllgaard B, Kvist LP, Costa Neto EM (2004) Implications and Borchsenius F, Balslev H (eds.) Botánica applications of folk zootherapy in the state of Económica de los Andes Centrales. Herbario Bahia, Northeastern Brazil. Sustainable Nacional de Bolivia, Universidad Mayor de San Development 12: 161–174. Andrés, Plural Editores, La Paz. pp. 412­433 Crespo JA (1982) Ecología de la comunidad de Cabral EL, Castro M (2007) Palmeras mamíferos del Parque Nacional Iguazú, Argentinas. Guía para el reconocimiento. Ed. Misiones. Revista MACN Ecología 3: 45­162. Lola, Buenos Aires. Crivos M, Martínez MR, Pochettino ML (2005) La Cadogan L (1992) Diccionario Mbya­Guaraní­ narrativa acerca del paisaje y del cambio Castellano. Biblioteca Paraguaya de ambiental entre los pobladores del área rural Antropología, Asunción 17: 1­211. del Municipio de Aristóbulo del Valle Cárdenas M (1989) Manual de Plantas (Misiones). Actas del I Congreso Argentino de Económicas de Bolivia. Editorial Amigos del Inmigración. IV Congreso de Historia de los Libro. 2 da edición. La Paz, Bolivia. Pueblos. de la Provincia de Santa Fe. Cebolla Badie MV (2009) El conocimiento y Dawson G, Gancedo O (1977) La palma pindó consumo de himenópteros, coleópteros y (Syagrus romanzoffianum) y su importancia lepidópteros en la cultura mbya­guaraní, entre los indios Guayaquí. Obra Cent. Mus. La Misiones, Argentina. Manual de Etnozoología Plata 2: 339­353. 3: 215­223. Defoliart GR 1995. Edible insects as Cebolla Badie MV (2013) Cosmología y minilivestock. Biodiversity and Conservation 4: naturaleza mbya­guaraní. Tesis de doctorado, 306–321. Facultad de Geografía e Historia, Universitat de Delgado C, Couturier G, Mathews P, Mejia K Barcelona. (2008) Producción y comercialización de la Cerda H, Martínez R, Briceño N, Pizzoferrato L, larva de Rhynchophorus palmarum Hermoso D, Paoletti M (1999) Cría, análisis (Coleoptera: Dryophtoridae) en la Amazonía nutricional y sensorial del picudo del peruana. Boletín Sociedad Entomológica cocotero Rhynchophorus palmarum Aragonesa 41: 407−412. (Coleoptera: Curculionidae), insecto de la Dounias E (2003) L’exploitation méconnu dieta tradicional indígena Amazónica. d’une ressource connue: la collecte des Ecotrópicos 12: 25­32. larves comestibles de charançons dans les Cerda H, Martinez R, Briceño N, Pizzoferrato L, palmiers­raphia au sud du Cameroun. In Les Manzi P, Ponzetta MT, Marin O, Paoletti MG Insectes dans la Tradition Orale. Edited by: (2001) Palm worm (Rhynchophorus palmarum) Motte­Florac E, Thomas JMC. Paris: Peeters, Traditional food in Amazonas , Venezuela­ Etnosciencies, 257­278. nutritional composition, small scale production and tourist palatability. Ecology of Food and Nutrition, 40: 13­32.

15 Araujo et al 2018. Management of pindo palm (Syagrus romanzoffiana, Arecaceae) in rearing of Coleoptera edible larvae by the Guarani of Northeastern Argentina Ethnobio Conserv 6:20

Dransfield J, Uhl NW, Asmussen CB, Baker WJ, Hill K, Kaplan H, Hawkes K, Hurtado AM (1985) Harley MM, Lewis CE (2008) Genera Men´s time allocation to Subsistence Work Palmarum: The Evolution and Classification among the Ache of Eastern Paraguay. Human of Palms. Kew publishing: Royal Botanic Ecology 13: 29­47. Gardens. Hurrell JA, Ulibarri EA, Delucci G, Pochettino ML Dufour DL (1987) Insects as food: A Case (2010) Biota Rioplatense XV. Frutas frescas, Study from the Northwest Amazon. American secas y preservadas. Editorial LOLA. Buenos Anthropologist 89: 383–397. Aires. Ellen R (2006) Local Knowledge and Hurtado AM, Hawkes K, Hill K, Kaplan H (1985) management of the sago palm (Metroxylon Female subsistence Strategies among Ache sagu rottboell) diversity in south central Hunter­Gatherers of Eastern Paraguay. Seram, Maluku, eastern Indonesia. Journal of Human Ecology doi: 10.1007/BF01531086. Ethnobiology, 26(2):258­298. INDEC (2015) Instituto Nacional de Estadística y Felipim AP (2001) O Sistema Agrícola Guarani Censos. Censo Nacional de Población, Mbyá e seus cultivares de milho: um estudo Hogares y Viviendas 2010: Censo del de caso na aldeia Guarani da Ilha do Cardoso, Bicentenario pueblos originarios, región município de Cananéia, SP. Dissertação para Nordeste Argentino. 1a ed. Ciudad Autónoma de obtenção do título de mestre em Ciências; Área Buenos Aires. de concentração: ciencias florestais. Piracicaba: Jacobsen TR (2003) Endangered Forest, ESALQ. Vanishing Peoples: Biocultural Diversity and Gatsuk LE, Smirnova OV, Vorontzova LI, Indigenous Knowledge. In: Galindo­Leal G., Zaugolnova LB, Zhukova LA (1980) Age states Gusmao do Camara I. (eds.). Atlantic forest of of plants of various growth forms: a review. South America. Biodiversity Status, Threats, and Journal of Ecology 68: 675­96. Outlook. Island Press, pp. 381­391 Giblin­Davis RM, Oehlschlager AC, Perez A, Keller HA (2008) Etnobotánica de Gries G, Gries R, Weissling TJ (1996) Chemical comunidades guaraníes de Misiones, and behavioral ecology of palm weevils Argentina. Valoración de la vegetación como (Curculionidae: Rhynchophorinae). Florida fuente de recursos. Tesis de doctorado en Entomologist 79: 153–167. Recursos Naturales, Facultad de Ciencias Giblin­Davis RM, Peña JE, Duncan RE (1994) Agrarias, Universidad Nacional del Nordeste. Lethal pitfall trap for evaluation of Keller HA (2010). Plantas relacionadas con semiochemical mediated attraction of tabúes del ciclo reproductivo de los Metamasius hemipterus sericeus (Coleoptera, guaraníes de Misiones, Argentina. Boletín de Curculionidae). Florida. Entomologist 77: 247­ la Sociedad Argentina de Botánica, 45(1­2):201­ 255. 208. Gragson TI (1992) The Use of Palms by the Keller HA (2014) Consideraciones fitonímicas Pume Indians of Southwestern Venezuela. a partir de dos mitos guaraníes sobre el Principes 36: 133­142. origen de Arecastrum romanzoffianum Guber R (2006) La etnografía, método, campo (Arecaceae). Suplemento Antropológico de la y reflexividad. Grupo editorial Norma. Buenos Universidad Católica de Asunción 49: 287­308. Aires, Bogotá. Keller HA, Prance GT (2008) Plants associated Hanboonsong Y, Jamjanya T, Durst PB (2013) with fish by Guaraníes of Misiones, Six­legged livestock edible insect farming, Argentina. Ethnobotany 20: 1­8. collecting and marketing in Thailand. Food Macía MJ, Armesilla PJ, Camara­Leret R, and Agriculture Organization of the United Paniagua­Zambrana N, Villalba S, Balslev H, Nations, Bangkok, Thailand. Pardo­de­Santayana M (2011) Palm Uses in Hernández­Pacheco F (1921) Escena pictórica Northwestern South America: A Quantitative con representaciones de insectos da época Review. The Botanical Review 77: 462–570. paleolítica. Boletín de la Real Sociedad Malinowski B (1922) Argonauts of the Western Española de Historia Natural 50: 62­77. Pacific. Ed. Dutton P. New York.

16 Araujo et al 2018. Management of pindo palm (Syagrus romanzoffiana, Arecaceae) in rearing of Coleoptera edible larvae by the Guarani of Northeastern Argentina Ethnobio Conserv 6:20

Martínez Crovetto RN (1968) La alimentación Oehlschlager AC (2016) Palm Weevil entre los indios guaraníes de Misiones. Pheromones–Discovery and Use. Journal of Etnobiológica 4: 1­24. chemical ecology 42: 617­630. Mayntzhusen F (2009) Los Aché Guayakí. Ed. Oehlschlager AC, Chinchilla CM, Castillo G, Junta de estudios históricos de Misiones. Gonzalez L (2002) Control of red ring disease Misiones, Argentina. by mass trapping of Rhynchophorus palmarum (Coleoptera: Curculionidae). Florida Messina FJ, Renwick JAA (1985) Mechanism of Entomologist 85: 507–513. egg recognition by the cowpea weevil Callosobruchus maculatus. Entomologia Oehlschlager AC, Chinchilla CM, Gonzalez LM Experimentalis et Applicata 37: 241–245. (1993a) Optimization of a pheromone baited trap for the American palm weevil Mercer CWL (1997) Sustainable production of Rhynchophorus palmarum (L.). Palm Oil. insects for food and income by New Guinea Research Institute of Malaysia Int Palm Oil Cong, villagers. Ecology of Food and Nutrition 36: 151­ Kuala Lumpur, Malaysia. 157. Oehlschlager AC, Chinchilla CM, Jiron LF, Mitsuhashi J (2017) Edible Insects of the Morgan B, Mexon RG (1993b) Development of World. CRC Press Taylor & Francis Group. an effective pheromone based trapping Japan. system for the American palm weevil, Moliniers P, Genes I (2003) Diccionario Rhynchophorus palmarum, in oil palm Guaraní. Diccionario usual de la lengua guaraní. plantations. J. Econ Entomol 86: 1381–1392. Editorial Visor, Argentina. Onore G (1997) A brief note on the edible Morin JP, Lucchini F, De Araujo JCA, Ferreina insect in Ecuador. Ecology of Food and JMS, Fraga LS (1986) Rhynchophorus control Nutrition, 36: 277­285. using traps made from oil palm cubes. Paniagua­Zambrana N, Bussmann RW, Macía Oléagineux 41: 57–62. MJ (2014) El Bosque Sí Tiene Valor: El uso de Moura JIL, Vilela de Resende ML, De Lima MM, palmeras en las comunidades campesinas e de Q. Santana DL (1991) Taticas para o indígenas de la región de Inambari, Madre de controle integrado de Rhynchophorus Dios, Perú. Ethnobotany Research and palmarum L. Centro de Pesquisas do Cacau applications 13 (3):001­081. (CEPEC), Bahía, Brazil. Paniagua­Zambrana N, Cámara­Leret R, Moura JIL, Vilela de Resende ML, Sgrillo RB, Bussmann RW, Macía MJ (2016) Nascimentl LA, Romano R (1990) Diferentes Understanding transmission of traditional tipos de armadilhas e iscas no controle knowledge across north­western South Rhynchophorus palmarum L. (Coleoptera: America: a cross­cultural study in palms Curculionidae). Agrotropica 2: 165–169. (Arecaceae). Botanical Journal of the Linnean Muafor FJ, Gall PL, Levang P (2014) Improving Society 182: 480–504. rural livelihoods through participative Placci LG, Di Bitetti M (2006) Situación research on the domestication and breeding ambiental en la Ecorregión del Bosque of the palm weevil larvae (Rhynchophorus Atlántico del Alto Paraná (Selva Paranaense). phoenicis Fabr.). The African palm weevil In: Brown A, Martínez Ortíz U, Acerbi M, project, pp 1­22. Corcuera J (eds.). La situación ambiental Müller F (1989) Etnografía de los Guaraní del Argentina 2005. FVS­Argentina. Buenos Aires, Alto Paraná. Ed. Societatis Verbi Divini. pp. 193­210. Argentina. Pochettino ML (2015) Botánica económica: las Noblick LR (2017) A revision of the genus plantas interpretadas según tiempo, espacio Syagrus (Arecaceae). Phytotaxa 294: 1­262. y cultura. Sociedad Argentina de Botánica, 1ª ed. C. A. Buenos Aires. Noelli FS (2004) La Distribución Geográfica de las evidencias Arqueológicas Guaraní. Revista de Indias 64: 17­34.

17 Araujo et al 2018. Management of pindo palm (Syagrus romanzoffiana, Arecaceae) in rearing of Coleoptera edible larvae by the Guarani of Northeastern Argentina Ethnobio Conserv 6:20

Ponzetta MT, Paoletti MG (1997) Insects as Souza AF, Martins FR (2005) Spatial variation food of the Irian Jaya populations. Ecology of and dynamics of flooding, canopy openness, Food and Nutrition 36: 321­346. and structure in a Neotropical swamp forest. Posey DA (1987) Ethnoentomological Survey Plant Ecology 180: 161­173. of Brazilian Indians. Entomol. Gener 12: 191­ Souza AF, Martins FR, Bernacci LC (2003) 202. Clonal growth and reproductive strategies of Ramos­Elorduy J (1997) Importance of edible the understory tropical palm Geonoma insects in the nutrition and economy of the brevispatha: an ontogenetic approach. people of rural areas in Mexico. J. Ecol. Food Canadian Journal of Botany 81: 101­112. and Nutr. 36: 347­366. Souza AF, Martins FR, Silva Matos DM (2000) Ramos­Elorduy J, Pino Moreno JM, Martínez Detecting ontogenetic stages of the palm Camacho VH (2009) Edible aquatic Coleoptera Attalea humilis in fragments of the Brazilian of the world with an emphasis on Mexico. Atlantic forest. Canadian Journal of Botany 78: Journal of Ethnobiology and Ethnomedicine 5:11. 1227­1237. Reitz R (1974) Palmeiras. Flora Ilustrada Svenning JC (2002) Crown illumination limits Catarinense. Parte 1: as plantas, fascículo: the population growth rate of a neotropical PALM. Herbário “Barbosa Rodrigues,” Itajaí, understorey palm (Geonoma macrostachys, Santa Catarina, Brazil. Arecaceae). Plant Ecology 159: 185­199. Renwick JAA (1989) Chemical ecology of Thomas R, De Franceschi D (2013) Palm stem oviposition in phytophagous insects. Cellular anatomy and computer­aided identification. and Molecular Life Sciences 45: 223–228. The Coryphoideae (Arecaceae). American Journal of Botany 100: 289–313. Rochat D, Malosse C, Lettere M, Ducrot PH, Zagatti P, Renou M, Descoins C (1991) Male­ Townsend PK (1974) Sago production in a New produced aggregation pheromone of the Guinea Economy. Human Ecology 2: 217­236. American palm weevil, Rhynchophorus Van Huis A (2003) Insect as food in sub­ palmarum (L.) (Coleoptera, Curculionidae): Saharan Africa. Insect and Science and its collection, identification, electrophysiological Application, 23(3):163­185. activity, and laboratory bioassay. J Chem Ecol Van Itterbeeck J,Van Huis A (2012) 17: 2127–2141. Environmental manipulation for edible insect Rosso CN, Scarpa GF (2012) Identificaciones procurement: a historical perspective. Journal botánicas de las plantas empleadas entre los of Ethnobiology and Ethnomedicine 8: 3. Mocovíes en la reducción San Javier durante Vaurie P (1970) Weevils of the tribe Sipalini el Siglo XVIII a partir de la obra de Florián (Coleoptera, Curculionidae, Paucke S J. In: Arenas P (ed) Etnobotánica en Rhynchophorinae) Part 1. The genera zonas áridas y semiáridas del cono sur de Rhinostomus and Yaccaborus. American Sudamérica. CEFYBO­CONICET, Buenos Aires, Museum Novitates, 2419:1­57. pp: 45­ 70. Schmitz PI (1991) Migrantes da Amâzonia: A Tradição Tupiguaraní. Kern AA (ed) Arqueologia pré­histórica do Rio Grande do Sul, Mercado Alberto, Porto Alegre, pp. 295­330.

Received: 11 September 2017 Accepted: 16 November 2017 Published: 5 December 2018

18