The host plants recorded for Heilipus species were compiled, based on a bibliographic survey and collection data on labels of material examined in entomological museums and collections. A plant was considered as a host for a Heilipus species only if there was evidence of immature stages developing in the plant tissue (e.g. seeds or trunk and branch bark), either in literature reports or in collection data of the material examined. Records of adults collected or found on a plant species without reference to rearing on plant tissue were not included.

A systematic search for references was conducted using academic databases with a range of key terms, including “Annonaceae borers”, “avocado weevils”, “Heilipus”, “Heilipus Annonaceae”, “Heilipus host plants”, “Heilipus Lauraceae”, “Lauraceae borers”, “Lauraceae seed predators” and “Lauraceae trunk borers”, amongst others. Additionally, references cited in agricultural reports, books, bulletins, catalogues, checklists, dissertations and scientific papers on the genus Heilipus published since approximately 1900 were tracked.

The main objective of this study is to provide a summary of the host plant-Heilipus species associations known to date, not to list all the instances where a given association has been reported in the literature or found in entomological collections. Therefore, each association is presented once per country, using the bibliographic reference where it was first mentioned. In many cases, the document mentioning an interaction for the first time is the only one available, but in the case of economically important plant genera such as Annona or Persea, there are many more reports. In some of these cases, more than one reference per country was provided to clarify the host plant variety or cultivar involved in the interaction or to improve the distribution records at least at the state/province or municipality level.

Occurrence information extracted from the bibliographic resources used (e.g. locality and coordinates when available) can be consulted through the link provided in the Data resources section.

A total of 931 specimens of the genus Heilipus were examined in 20 natural history collections in Brazil (20 specimens), Colombia (249), Mexico (142), United Kingdom (118) and United States (402). These collections are listed below:

CEAH Coleção Entomológica Adolph Hempel, Instituto Biológico, São Paulo, Brazil.

CEAM Colección Entomológica del Colegio de Postgraduados, Campus Montecillo, State of Mexico, Mexico.

CEBAJ-INIFAP Colección Nacional de Insectos del Campo Experimental Bajío del INIFAP, Centro de Investigación Regional Centro, Guanajuato, Mexico.

CEUA Colección de Entomología de la Universidad de Antioquia, Antioquia, Colombia.

CEUNP Colección de Entomología de la Universidad Nacional Sede Palmira, Valle del Cauca, Colombia.

CNIN Colección Nacional de Insectos del Instituto de Biología, Universidad Nacional Autónoma de México, Ciudad de México, Mexico.

CNRF-DGSV Colección de Entomología y Acarología del Centro Nacional de Referencia Fitosanitaria, Dirección General de Sanidad Vegetal - SENASICA, State of Mexico, Mexico.

CTNI Colección Taxonómica Nacional Luis María Murillo, Centro de Investigación Tibaitatá de AGROSAVIA, Cundinamarca, Colombia.

IAvH-E Colección de Entomología del Instituto de Investigación de Recursos Biológicos Alexander von Humboldt, Boyacá, Colombia.

ICN Colección de Coleoptera del Instituto de Ciencias Naturales, Universidad Nacional Sede Bogotá, Bogotá, D. C., Colombia.

IEXA Colección Entomológica del Instituto de Ecología, A.C., Veracruz, Mexico.

LEUC Colección del Laboratorio de Entomología de la Universidad de Caldas, Caldas, Colombia.

MEFLG Museo Entomológico Francisco Luis Gallego, Universidad Nacional Sede Medellín, Antioquia, Colombia.

MEMB Museo Entomológico Marcial Benavides, Cenicafé, Caldas, Colombia.

MPUJ_ENT Colección Entomológica del Museo Javeriano de Historia Natural, Pontificia Universidad Javeriana, Bogotá, D. C., Colombia.

MUSENUV Museo de Entomología de la Universidad del Valle, Valle del Cauca, Colombia.

MZFC Museo de Zoología Alfonso L. Herrera, Facultad de Ciencias, Universidad Nacional Autónoma de México, Ciudad de México, Mexico.

NHMUK Natural History Museum, London, England, United Kingdom.

UNAB Museo Entomológico de la Facultad de Ciencias Agrarias, Universidad Nacional Sede Bogotá, Bogotá, D. C., Colombia.

USNM Smithsonian National Museum of Natural History, Department of Entomology, Washington, D.C., United States of America.

Only 40% of the examined specimens had information on their habits and host plants. Furthermore, only 7% of these 40% corresponded to plants other than avocado. Consequently, occurrence data from only 85 specimens are presented (Data resources section), providing information on 12 host plant associations not previously reported in the literature. These 85 specimens belong to 13 locality records for 10 Heilipus species and are deposited at the CEAH, MEFLG and USNM.

All botanical names and plant synonyms used correspond to the names and taxonomic treatment accepted in The Word Flora Online (WFO 2024) at the time of access.

The data underpinning the analysis reported in this paper are deposited in the Dryad Data Repository at https://doi.org/10.5061/dryad.0cfxpnwbn.

Seed predators

(Fig. 1A–D)

The biology of spermophagous species begins with the female boring into the fruit to deposit her eggs as close to the seed as possible. This oviposition occurs in fruits that are attached to the tree (Downey et al. 2020; Rodríguez-Sánchez et al. 2022), placing this genus in the category of pre-dispersal seed predators. In small fruits, such as those of the genera Aniba Aubl. or Ocotea Aubl. (Lauraceae), oviposition is common towards the final development of the fruit (Spironello et al. 2004), ripe or unripe (Vernalha 1953; Pessotto et al. 2021). In larger fruits, such as avocado, oviposition also occurs while the fruit is attached to the tree, but often during growth; for example, a high incidence of damage by H. lauri (Fig. 1D) was observed when avocado fruits reached 4 to 5 cm in diameter (Castañeda-Vildózola et al. 2017) or a length between 3 and 12 cm (Caicedo et al. 2010). Fruits with small oviposition punctures (Bravo 2008), perforations or holes in the epidermis with the presence of a black or dark circular scab (Caicedo et al. 2010) are signs of the infestation by species of the genus Heilipus. From one to three eggs per fruit have been reported in avocado fruits attacked by H. lauri (Castañeda-Vildózola et al. 2013) and H. trifasciatus (Santos-Murgas et al. 2014). Pessotto et al. (2021) also reported one to three eggs per fruit in Ocotea puberula (Rich.) Nees fruits infested by H. draco, with one egg per fruit being the most common finding. In avocado fruits, whitish exudates around the perforations are indicatives of infestation by these weevils (Castañeda-Vildózola et al. 2013).

The emerging larva feeds on the endosperm, where it completes all its larval development. Larvae are cannibalistic and this behaviour usually results in only one larva per seed (Castañeda-Vildózola et al. 2017; Pessotto et al. 2021; Rodríguez-Sánchez et al. 2022). However, it is possible to find two or up to four larvae in large seeds, such as those of avocado (Dietz and Barber 1920; Santos-Murgas et al. 2014; Castañeda-Vildózola et al. 2017). Although larval development inside the seed often causes abortion or premature drop of the infested fruit (Peña 1998), in some cases, the fruit remains attached to the tree even when the pupa or adult is fully developed (Castañeda-Vildózola et al. 2009). The pupal stage also occurs inside the seed (Fig. 1C). Upon completion of metamorphosis, the adult makes a hole with its mandibles to emerge from the seed (Vanin and Gaiger 2005; Santos-Murgas et al. 2014; Díaz-Grisales et al. 2017). This frequently occurs when the fruit has fallen to the ground (Vernalha 1953; Pessotto et al. 2021). Adult feeding targets in spermophagous and trunk-boring species, include leaves, buds, tender shoots, young branches and growing fruits without affecting the seeds. Damage to these structures is considered secondary and of no economic importance (Wolfenbarger 1948; Lourenção et al. 1984; Castañeda-Vildózola et al. 2010; Díaz-Grisales et al. 2017).

Damage rates, at least for the species for which this has been documented, are highly variable. Reported incidences range from 0.06% of O. puberula fruits infested by H. draco (Fig. 1B) in Panama (Downey et al. 2020), 16% of Damburneya ambigens (S.F. Blake) Trofimov seeds damaged by H. albomaculatus (Champion) in Mexico (Rodríguez-Sánchez et al. 2022), 42.5% of wild avocado seeds injured by larvae of H. trifasciatus in Panama (Dietz and Barber 1920), 75% of Aniba rosodora Ducke fruits attacked by H. odoratus in Brazil (Morais et al. 2009) and up to 80% of avocado fruits infested by H. lauri in backyard orchards in Mexico (Castañeda-Vildózola et al. 2013). Infestation by spermophagous species of Heilipus can affect seed germination because the larvae consume the embryo and its reserves, leaving only the seed integument (Gómez and Toro 2007; Pessotto et al. 2021). However, seeds can germinate if the embryo is not damaged (Barber 1919; Spironello et al. 2004; Bravo 2008).

Trunk borers

(Fig. 1E–H)

The habits and biology of the trunk borers of the genus Heilipus are known primarily from the species that attack avocado in the Americas. Similar habits and behaviour, although poorly documented, have been observed in the species that bore into the trunks of the family Annonaceae. The female lays eggs in the bark, usually at the base of the tree, in the root collar area (Wolfenbarger 1948; Lourenção et al. 2003). Oviposition is most common at the base of the tree, but can also occur in the lower branches and thick roots near or below the ground (Lourenção et al. 2003; Moura et al. 2006; Rubio et al. 2009). In avocado, oviposition and damage caused by Heilipus species have been documented on trees ranging from 0.5 years old (Wolfenbarger 1948) and up to more than 30 years old (Rubio et al. 2009). In Florida orchards (USA), most signs of infestation by H. squamosus (Fig. 1H) larvae were observed in the first 15.24 cm (6 inches) above the ground in small avocado trees with a diameter of 7.62–15.24 cm (3–6 inches) (Wolfenbarger 1948). In the State of Mexico (Mexico), oviposition by H. albopictus (Fig. 1F) was recorded 40 cm above the ground in stems of Mexican criollo avocado (Castañeda-Vildózola et al. 2010). In the Department of Tolima (Colombia), the incidence of H. elegans larvae was higher at the base of common or criollo avocado trees that were older than 30 years and exceeded 15 m in height (Rubio et al. 2009). Signs of infestation by these borers are reddish-orange masses of faeces and exudates on the trunk caused by larval feeding, usually near or at ground level, in the shaded areas of the trunk and branches (Wolfenbarger 1948; Rubio et al. 2009; Castañeda-Vildózola et al. 2010). The masses tend to crumble and be washed away by rain (Wolfenbarger 1948).

After emerging from the egg, the larvae begin to feed on the subcortical tissues (Fig. 1E), between the bark and the vascular cambium layer, leaving a gallery as they feed, plugging or blocking the gallery with their excrement (Lourenção et al. 2003; Wolfenbarger 1948). From one (Wolfenbarger 1948) to up to 30 larvae (Rubio et al. 2009) have been found in a single avocado trunk infested with borers of the genus Heilipus. Once larval development is complete, pupation occurs in a cell previously built by the larva between the bark and the wood of the tree (Castañeda-Vildózola et al. 2010). Finally, the adult emerges from the trunk. Losses and incidence rates reported vary from 8% to 10% of the trees in an avocado orchard infested by H. squamosus in Florida, USA (Wolfenbarger 1948); 30% of avocado trees killed by feeding of H. rufipes larvae in Ceará, Brazil (Lourenção et al. 2003); and 49.1% of avocado trunks infested by H. elegans larvae in orchards from Tolima, Colombia (Rubio et al. 2009). In contrast, there are no records of the incidence, percentage of damage or number of larvae found in trunks for the species that attack plants in the family Annonaceae. Symptoms of infestation by trunk borers of the genus Heilipus include yellowing of leaves, defoliation, drying of branches, girdling, wilting and even death of affected trees (Wolfenbarger 1948; Lourenção et al. 1984, 2003; Rubio et al. 2009; Castañeda-Vildózola et al. 2013).

Species in the genus Heilipus are associated with at least 13 plant genera belonging to the families Annonaceae (one genus) and Lauraceae (12 genera). These associations are summarised in Table 1 and described in detail below.

Aiouea Aubl. (Lauraceae)

In Barro Colorado Island, Panama, Gripenberg et al. (2019) recorded the emergence of adults of H. draco from seeds of Cinnamomum triplinerve, one of the synonyms of the species Aiouea montana (Se.) R. Rohde.

Aniba Aubl. (Lauraceae)

Larvae of H. odoratus feeding on seeds of A. rosodora Ducke in Manaus, Amazonas State, Brazil (Vanin and Gaiger 2005). In Colombia, Gómez and Toro (2007) reported that an unidentified species of the genus Heilipus attacks the seeds of Aniba perutilis Hemsl. in Andean forests. In addition, four specimens of H. longirostris (Díaz-Grisales et al. 2021) and two of a verified new Heilipus species (Heilipus sp. nov. VDG6) were obtained from seeds of Aniba sp. collected in San Francisco, Department of Antioquia. The two specimens of Heilipus sp. nov. VDG6 are deposited at the MEFLG. With 20 species, Aniba is one of the five richest genera of Lauraceae in Colombia (Raz and Agudelo Zamora 2023).

Annona L. (Annonaceae)

The association of Heilipus species with this genus and this family has been reported only in trunks and only in states of the south and southeast regions of Brazil. Heilipus gibbus has been recorded damaging the trunks of soursop (A. muricata L.) and the hybrid atemóia (A. cherimola Mill. × A. squamosa L.) in the States of Distrito Federal and São Paulo (Vanin and Bená 2015). Heilipus lactarius on trunks of biribá (A. mucosa Jacq.), fruta-do-conde (A. reticulata L.) and araticum-do-mato (A. sylvatica A. St.-Hil.) in Minas Gerais, Rio de Janeiro and São Paulo (Costa-Lima 1956; Silva et al. 1968). Heilipus velamen has been found in trunks of A. reticulata in the States of Espírito Santo, Rio de Janeiro and São Paulo (Costa-Lima 1956; Silva et al. 1968). There are also reports of H. catagraphus damaging the base of the trunks of A. mucosa (Silva et al. 1968), A. muricata (Moura et al. 2006; Braga Sobrinho et al. 2011) and A. reticulata (Ihering 1909) in Brazil. However, these records may be the result of erroneous identifications, as H. gibbus was frequently misidentified as H. catagraphus (Vanin and Bená 2015). According to Vanin and Bená (2015), it is possible that H. gibbus is exclusively associated with plant trunks of the family Annonaceae, while H. catagraphus is associated with the trunks of the family Lauraceae.

Annona mucosa is native to the southeast and other regions of Brazil (Flora e Funga do Brasil 2024), whereas A. reticulata is cultivated in several States, including Minas Gerais, Rio de Janeiro and São Paulo (Flora e Funga do Brasil 2024). Annona sylvatica, an endemic species to Brazil, is less widely distributed than A. mucosa, but is also present in the southeast and other regions of the country (Flora e Funga do Brasil 2024).

Beilschmiedia Nees. (Lauraceae)

In Barro Colorado Island, Panama, 116 individuals of H. draco emerged from 3404 fruits of B. tovarensis (Klotzsch & H. Karst. ex Meisn.) Sach. Nishida collected by Downey et al. (2020) over a period of two years.

Caryodaphnopsis Airy Shaw. (Lauraceae)

Two additional adults of Heilipus sp. nov. VDG6 were found at the MEFLG. Based on the associated label data, these individuals emerged from seeds of C. cogolloi van der Werff, a species endemic to Colombia, collected in the Municipality of San Luis, Antioquia. Seven species of Caryodaphnopsis are found in Colombia, three of which are endemic (Mendoza-Cifuentes et al. 2023). The distribution of C. cogolloi is limited to the Reserva Natural Cañón del Río Claro El Refugio in the Department of Antioquia, where it is critically endangered due to timber overexploitation (Polanco et al. 2014).

Cinnamomum Schaeff. (Lauraceae)

Examination of the material deposited at the USNM yielded ten specimens of H. draco, which, according to their labels, emerged from seeds of the cinnamon tree (C. verum J. Presl) from Trinidad and Tobago. Similarly, 20 adults of the same species were found at the CEAH, which emerged from seeds of C. verum collected in the Municipality of Campinas, São Paulo State, Brazil. For H. draco, these two findings represent a new host plant record. Heilipus mirus is another species associated with the genus Cinnamomum. It causes damage to the bark of camphor trees (C. camphora (L.) J. Presl) in Jamaica. The association between H. mirus and C. camphora rectifies an error that arose more than a century ago. In 1905, William Fawcett, the director of Jamaica’s Public Gardens and Plantations, sent Leland Ossian Howard, then chief of the Bureau of Entomology of the United States Department of Agriculture, samples of an insect that was attacking young camphor trees at the Cinchona Botanical Garden in Jamaica. Regarding the samples, Howard informed Fawcett that “…Mr. Schwarz [probably referring to the entomologist Eugene Amandus Schwarz] reports that the weevil is Hilipus [sic] elegans, Guérin of the family Curculionidae.” Fawcett (1906) published this information in the Bulletin of the Jamaica Department of Agriculture. Since then, it is believed that H. elegans, a species known to bore avocado trunks in Colombia (Rubio et al. 2009, see below), can also cause damage to C. camphora. However, one of the specimens received by Howard was physically examined at the USNM by the first author of this work and it was discovered that it did not belong to the species H. elegans, but to H. mirus. Therefore, the only confirmed host plant so far for H. elegans is P. americana, while the association of H. mirus with C. camphora represents a new report of habit and host plant for this Heilipus species.

Clinostemon Kuhlm. & A. Samp. (Lauraceae)

A species close to H. hopei Boheman was obtained by Costa-Lima (1956) from a seed of Licaria mahuba from Pará, Brazil. Currently, L. mahuba is considered a synonym of Clinostemon mahuba (A. Samp.) Kuhlm. & Samp. (Flora e Funga do Brasil 2024).

Damburneya Raf. (Lauraceae)

Three spermophagous species of Heilipus have been recorded in this genus of plants in the tropical rainforest of Los Tuxtlas Biosphere Reserve, situated within the Mexican State of Veracruz: H. albomaculatus in seeds of D. ambigens (S.F. Blake) Trofimov and D. gentlei (Lundell) Trofimov and H. draco and H. guttiger (Champion) in seeds of D. salicifolia (Kunth) Trofimov & Rohwer (Rodríguez-Sánchez et al. 2022). Additionally, from Mexico, the USNM houses a specimen of H. albovenosus (Champion) (Fig. 1A) obtained from a fruit of D. coriacea (Sw.) Trofimov & Rohwer from the Municipality of Tampico, State of Tamaulipas. The native range of D. coriacea extends from Mexico to Central America and from southern Florida to the Caribbean (WFO 2024). This is the first time that the habit and host plant of H. albovenosus have been reported.

In Costa Rica, five adults of a verified new species of Heilipus (Heilipus sp. nov. VDG1) and one of H. guttiger emerged from seeds of D. salicina (C.K. Allen) Trofimov & Rohwer collected in Monteverde, Puntarenas Province. In addition, a specimen of the trunk borer H. squamosus was found in wood of D. coriacea in the locality of Noble, Georgia, United States. The reports of H. guttiger in D. salicina and H. squamosus in D. coriacea represent new host plant records for these Heilipus species; both specimens, along with the five Heilipus sp. nov. VDG1, are deposited at the USNM.

Mespilodaphne Nees & Mart. ex Nees. (Lauraceae)

In Santa Rosa National Park, Guanacaste Province, Costa Rica, H. draco is a seed predator of M. veraguensis (Meisn.) Rohwer (Janzen 1987).

Mezilaurus Kuntze ex Taub. (Lauraceae)

Five adults of H. longirostris were obtained from seeds of an unidentified species of Mezilaurus collected in the Municipality of San Luis, Department of Antioquia, Colombia; these specimens are deposited at the MEFLG. This finding represents a new host plant genus record for H. longirostris. Notably, the genus Mezilaurus has only four recorded species in Colombia (Raz and Agudelo Zamora 2023).

Nectandra Rol. ex Rottb. (Lauraceae)

Within this genus, Heilipus species have been reported in both seeds and trunks. Two adults of H. guttiger emerged from seeds of N. turbacensis (Kunth) Nees collected in the rainforest of Los Tuxtlas, Veracruz, Mexico (Rodríguez-Sánchez et al. 2022). In Barro Colorado Island, Panama, H. draco has been recorded on seeds of N. cissiflora Nees (Gripenberg et al. 2019; Downey et al. 2020) and N. lineata (Kunth) Rohwer (Downey et al. 2020). In Brazil, Sanz-Veiga et al. (2024) obtained adults of H. draco and H. vividaensis from seeds of N. angustifolia (Schrad.) Nees & Mart. collected in the Municipality of Guapiara, State of São Paulo. They also recorded the occurrence of H. draco in seeds of N. angustifolia from Piracicaba, also in São Paulo State (Sanz-Veiga et al. 2024). In the State of Minas Gerais, Carvalho et al. (2009) reported an undetermined species of the genus Heilipus as a seed predator of N. nitidula Nees & Mart. in the Municipality of Poços de Caldas. Finally, H. catagraphus has been documented as a trunk borer of N. venulosa Meisn., commonly known as canelinha, in Brazil (Bondar 1915; Costa-Lima 1956; Silva et al. 1968). Nectandra venulosa is endemic to Brazil, only having been recorded from the State of Minas Gerais (Flora e Funga do Brasil 2024).

Ocotea Aubl. (Lauraceae)

Amongst the genera of Lauraceae, Ocotea has the largest number of records of spermophagous species of Heilipus, especially H. draco (Fig. 1B) and other morphologically similar species. In Monteverde, Puntarenas Province, Costa Rica, one adult of H. empiricus (Pascoe) was obtained from a seed of O. glaucosericea Rohwer and six other adults of Heilipus sp. nov. VDG1 from seeds of O. floribunda (Sw.) Mez; these seven specimens are deposited at the USNM. The occurrence of H. empiricus in O. glaucosericea seeds is a new record of the habit and host plant of this species of Heilipus. In Barro Colorado Island, Panama, Gripenberg et al. (2019) obtained an adult of an undetermined Heilipus species (Heilipus sp. cur15SG) from seeds of O. whitei Woodson. In the same locality, Downey et al. (2020) recorded the emergence of H. draco specimens from seeds of O. leptobotra (Ruiz & Pav.) Mez, O. oblonga (Meisn.) Mez and O. puberula (Rich.) Nees.

In Brazil, H. draco adults have also been obtained from O. puberula seeds collected in the Municipality of Taquaruçu do Sul, Rio Grande do Sul (Pessotto et al. 2021) and from O. porosa (Nees & Mart.) Barroso seeds collected in the Canoinhas Region, State of Santa Catarina (Hirano 2004). Heilipus parvulus is another species that has been documented as a seed predator of O. porosa in Ponta Grossa, Paraná (Vernalha 1953). Additionally, in the State of Paraná, Sanz-Veiga et al. (2024) obtained adults of H. vividaensis from fruits of O. puberula collected in the Municipality of Coronel Vivida. In Argentina, seeds of O. diospyrifolia (Meisn.) Mez (Bravo and Sallenave 2003) and O. puberula (Bravo and Zunino 1998) infested with larvae of an undetermined species of Heilipus were collected in Brasilera Island, an area located at the confluence of the Paraná and Paraguay Rivers. Finally, only one species has been reported in the trunks of Ocotea. According to Costa-Lima (1956) and Silva et al. (1968), the larvae of H. peplus (Fig. 1G) bore canela-preta (O. catharinensis Mez) in Rio Grande do Sul, Brazil.

Persea Mill. (Lauraceae)

This is the plant genus from which Heilipus has traditionally been recorded, mainly because of the damage that some of its species cause to the seeds and trunks of avocado (P. americana), one of the most economically important species of the family Lauraceae.

Seed predators of the genus Persea include the species H. lauri (Fig. 1C, D), H. pittieri and H. trifasciatus. Another species documented on avocado seeds is Heilipus montei Costa-Lima, a synonym of H. parvulus according to Kuschel (1958). Heilipus montei was described, based on four specimens that were purportedly obtained from avocado fruits collected in Conceição do Serro, Minas Gerais State, Brazil (Costa-Lima 1935). Nevertheless, this association is suspect as it has not been corroborated or found again since the description of H. montei by Costa-Lima in 1935.

In Mexico, larvae and adults of H. lauri have been found in seeds of commercial cultivars and varieties of P. americana (Schoenherr 1845; Barber 1919) in the States of Chiapas, Guerrero, Hidalgo, Mexico, Morelos, Oaxaca, Puebla and Veracruz (Castañeda-Vildózola et al. 2013; Vázquez et al. 2017). Amongst the commercial cultivars are Choquette, Colín V-33, Fuerte and Hass (Salgado and Bautista 1993; Medina-Quiroz et al. 2010). The avocado varieties include criollo or Mexican avocados (P. americana var. drymifolia (Schltdl. and Cham.) S.F. Blake) (Castañeda-Vildózola et al. 2017) and pahuas (P. americana var. americana) (Palacios-Torres et al. 2016). Furthermore, Castañeda-Vildózola et al. (2009) obtained H. lauri adults from seeds of the species P. schiedeana Nees collected in the Municipality of Huatusco, State of Veracruz, Mexico. In Colombia, H. lauri has been recorded in the fruits of P. americana (Gallego 1949) from the cultivars Hass (Caicedo et al. 2010) and Trinidad (Cárdenas 1984a) in the Departments of Antioquia, Caldas, Cauca, Cundinamarca, Quindío, Risaralda, Tolima and Valle del Cauca (Gallego 1949; Díaz-Grisales et al. 2017). In addition, Cárdenas (1984b) pointed out that, in the Viejo Caldas (former Colombian Department that existed between 1905 and 1966 and was comprised of the current Departments of Caldas, Quindío and Risaralda; López-Pacheco (2011)), H. lauri populations were more numerous and aggressive in native avocados, where trees with all fruit damaged were detected. Possibly, the native avocados mentioned by Cárdenas (1984b) may have been related to the West Indian race (P. americana var. americana), as criollo or native Colombian avocados are typical of this variety of P. americana (Bernal and Díaz 2020).

Like H. lauri, H. pittieri also feeds on seeds of P. americana (González-Herrera 2003) and P. schiedeana (Barber 1919) in its larval stage. Barber (1919) obtained four adults of H. pittieri from seeds of Persea pittieri Mez (one of the synonyms of P. schiedeana) from San José, Costa Rica; these adults are deposited at the USNM and represent the holotype, allotype and two paratypes of H. pittieri. Castañeda-Vildózola et al. (2013) mentioned damage by H. pittieri to the fruits of P. americana cv. Hass in Costa Rica; however, the authors did not provide the precise location of the finding. Similarly, Maes (2004) reported the occurrence of H. pittieri on avocado trees in Atlantic Nicaragua, yet he did not specify the cultivar or variety of avocado on which the observation was made.

Conversely, larvae and adults of H. trifasciatus have only been found in fruits of P. americana (Dietz and Barber 1920). In Colombia, the occurrence of this species attacking avocado seeds has been reported in the Municipalities of Acandí (Chocó), Palmira (Valle del Cauca) and Mistrató (Risaralda) (Díaz-Grisales et al. 2020). The report from Acandí is the only one that mentions two adults of the species emerging from seeds of native or criollo avocado (P. americana var. americana) (Díaz-Grisales et al. 2020). The avocado variety or cultivar from which the specimens were collected was not specified in the case of the Municipalities of Palmira and Mistrató. In Panama, Dietz and Barber (1920) found wild avocado seeds infested with H. trifasciatus larvae in Frijoles, Canal Zone. Santos-Murgas et al. (2014) reported damage by H. trifasciatus larvae in common or criollos avocado seeds from the community of Altos del María, Sorá, Panama. As in the case of Colombia, it is likely that the wild and criollo avocado trees mentioned by Dietz and Barber (1920) and Santos-Murgas et al. (2014) belong to or are close to the West Indian race (P. americana var. americana). González-Herrera (2003) reported that H. trifasciatus damages avocado fruits in Costa Rica, but he did not specify the variety or cultivar, nor the location where the observations were made. Finally, Maes and O’Brien (1990) reported the presence of H. trifasciatus in the Departments of Carazo, Chontales and Masaya (Nicaragua) and mentioned that it is a phytophagous species recorded on the genus Persea; however, they did not indicate with which species of Persea it is associated in that country.

To date, seven species of trunk boring Heilipus cause damage to the trunks and branches of varieties and commercial cultivars of P. americana. In the State of Florida, United States, Wolfenbarger (1948) found larvae of H. squamosus boring into the bark at the base of avocado trees, as well as adults feeding on fruits without affecting the seeds; however, the author did not specify the avocado variety or cultivar on which he made the observations. Heilipus squamosus (Fig. 1H), the sole species of Heilipus present in the United States, was long misidentified as H. apiatus (Olivier). Its presence is currently documented in 15 States across the south-eastern, south-western and mid-western regions of the country, though only in Florida has it been reported causing damage to avocado trees (Anzaldo and Díaz-Grisales 2022). In Mexico, H. albopictus larvae (Fig. 1E) were found in the stems of P. americana var. drymifolia in Ixtapan de la Sal and in Hass and Fuerte avocados in Coatepec Harinas, State of Mexico; damage in Hass and Fuerte cultivars was limited to the rootstock of Mexican criollo avocado (P. americana var. drymifolia) (Castañeda-Vildózola et al. 2010). In Costa Rica, González-Herrera (2003) reported H. elegans in association with avocado trees, but he did not specify the location or the variety or cultivar on which the observations were made. Reports of H. elegans boring in the inner bark of camphor trees (C. camphora) in Jamaica are common in the literature of the genus Heilipus (Fawcett 1906; Schwarz 1907; Rubio et al. 2009; Santos-Murgas et al. 2014); however, it is worth mentioning that they correspond to misidentifications of H. mirus (see above, genus Cinnamomum).

In Colombia, H. elegans is known to bore into the trunks of P. americana in its larval stage. In the Municipality of Fresno, Department of Tolima, Rubio et al. (2009) recorded damage by this species on both common or criollo trees and the cultivars Booth 8, Choquette, Lorena, Santana and Trinidad (Rubio et al. 2009). Additionally, in Colombia, larvae and adults of H. leopardus have been found inside the trunks of Hass avocado trees in the Municipalities of Urrao (Antioquia) and Manzanares (Caldas) (Díaz-Grisales 2019). In addition, 30 adults of H. fassli (Voss) that emerged from Hass avocado trunks in Urrao are housed at the MEFLG. This is the first report of the habit and host plant of H. fassli, which joins the list of Heilipus species that attack avocado in Colombia and shares the habit of boring trunks with H. elegans and H. leopardus. In Brazil, H. catagraphus larvae bore into the subcortical tissues of avocado (Bondar 1915; Costa-Lima 1956; Silva et al. 1968). Furthermore, H. rufipes larvae have been found in the trunks of avocado cultivar Bertanha in São Benedito, State of Ceará, Brazil (Lourenção et al. 2003). Finally, Silva et al. (1968) mentioned that H. elegans bores avocado branches and trunks in the State of Santa Catarina, Brazil. However, Vanin and Bená (2015) suggested that this information may correspond to a misidentification, since Wibmer and O’Brien (1986) did not mention the presence of H. elegans in Brazil in their South American catalogue.

Nine major evolutionary lineages in Lauraceae have been proposed by Rohwer (2000), Chanderbali et al. (2001), Rohwer and Rudolph (2005) and Song et al. (2017): Hypodaphnis, Cryptocarya group, Cassytha, Neocinnamomum, Caryodaphnopsis, Mezilaurus group, Persea group, Cinnamomeae and Laureae. The interactions recorded so far between Heilipus and 12 genera of the family Lauraceae occur in five of these nine lineages: Cinnamomeae (Aiouea, Aniba, Cinnamomum, Damburneya, Mespilodaphne, Nectandra and Ocotea), Mezilaurus group (Clinostemon and Mezilaurus), Persea group (Persea), Caryodaphnopsis (Caryodaphnopsis) and Cryptocarya group (Beilschmiedia) (Table 1). Of the 33 Lauraceae species reported here as host plants for the genus Heilipus, 27 belong to the Cinnamomeae clade, two to the Persea group, two to the Mezilaurus group, one to the Caryodaphnopsis clade and one to the Cryptocarya group (Table 1). In terms of the number of Heilipus species, the Cinnamomeae clade occupies the first place with at least 15 associated Heilipus species, four trunk borers and the rest seed borers. The Persea group is the second lineage with more Heilipus species recorded, counting three seed borers and seven trunk borers. Four spermophagous species feed on the remaining three lineages: two species on the Mezilaurus group, one species on the Caryodaphnopsis clade and one species on the Cryptocarya group (Table 1).

The genus Heilipus has close ecological associations with magnoliids of the families Lauraceae (Laurales) and Annonaceae (Magnoliales). To date, the habits and host plants of 24 of the 90 species described in the genus are known, with information for four of these species being first reported in this study. Of these 24 species, 12 are seed borers and 12 are trunk borers. The trunk and branch boring habit could be considered more generalist, occurring in both Annonaceae and Lauraceae, whereas the seed boring habit is more specialised and exclusive to the family Lauraceae. With seeds of at least 30 species of Lauraceae in which the immature stages of Heilipus species develop, these weevils should be considered one of the most important pre-dispersal seed predators of this botanical family in the Americas. Although some authors assert that Heilipus larval feeding severely affects seed germination, especially if the embryo is damaged (Gómez and Toro 2007; Pessotto et al. 2021), the role of these weevils may not be entirely detrimental. Larval development of Heilipus species may facilitate seed germination, as observed by Sánchez-Garduño (1995) in Damburneya ambigens from Los Tuxtlas Region. In that case, seeds infested by H. albomaculatus germinated faster than those infested by Pagiocerus frontalis (Fabricius) (Curculionidae, Scolytinae, another pre-dispersal seed predator) and undamaged seeds (Sánchez-Garduño 1995). However, the fitness of seedlings derived from seeds where Heilipus completed metamorphosis without affecting the embryo remains unknown. Gómez and Toro (2007) noted that some seeds of Aniba perutilis not severely damaged by Heilipus larvae can germinate, but the seedlings soon die due to the lack of reserves. Unfortunately, this observation was not experimentally verified.

The oligophagous feeding behaviour of Heilipus was documented by Díaz-Grisales et al. (2021), who reported that some species within the genus feed on plants from different genera of the family Lauraceae. This study expands on that finding, supporting that oligophagy is a very common pattern in this group of weevils, particularly amongst seed borers. Nine of the seed borers listed in Table 1 are associated with more than one host plant (H. albomaculatus, H. draco, H. guttiger, H. lauri, H. longirostris, H. pittieri, Heilipus sp. nov. VDG1, Heilipus sp. nov. VDG6 and H. vividaensis), while the others have been observed on only one. Amongst the 12 trunk-borer species whose host plants are summarised here, four are associated with more than one host (H. catagraphus, H. gibbus, H. lactarius and H. squamosus), while the remaining eight have been detected on a single plant species (Table 1). This does not imply that the species documented on a single host plant lack additional hosts; rather, it indicates a need for more biological and ecological data, both on labels and in publications. The labels of Heilipus specimens held in scientific collections often lack biological data.

Oligophagy in trunk borers

Amongst the trunk borers reported on more than one host are H. gibbus and H. lactarius, which specialise in Annona species. The remaining two species, H. catagraphus and H. squamosus, have been recorded on trunks of the family Lauraceae. Notably, the hosts of H. catagraphus, H. lactarius and H. squamosus include native or endemic plants, as well as economically important plants cultivated near to the former. This suggests that Heilipus trunk borers may colonise alternative plant species in response to the loss of their primary host. For example, the anthropogenic pressure on the Atlantic Forest of Brazil due to massive agricultural expansion, industrialisation and urbanisation (Ribeiro et al. 2011) may have driven H. catagraphus and H. lactarius to migrate from native or endemic plants to related cultivated ones. Alternatively, trunk borers could be simply responding to a strong attraction to volatile organic compounds emitted by related plants growing in monocultures (avocado or Annona crops). This attraction can result in oviposition and the development of immature stages in these alternative hosts, as has been observed in avocado crops in some countries of the Americas (see below).

Nonetheless, a strong attraction to an alternative host does not always result in oviposition or larval development. For instance, Lourenção et al. (1984) observed H. catagraphus adults feeding on young avocado fruits of the Fortuna cultivar in a commercial orchard in Barão Geraldo, State of São Paulo. However, no larvae or immature stages were found in the avocado trunks and the adults disappeared two months later without any control measures (Lourenção et al. 1984). Similarly, Reis et al. (2018) recorded adults of Heilus freyreissi (Boheman), another member of the subtribe Hylobiina, feeding on tender lateral branches, central leaf veins, inflorescences, peduncles and young fruits of avocado trees (cultivars Margarida, Breda and Hass) planted in Rio Paranaíba, State of Minas Gerais. Despite these observations, the study does not mention the presence of larvae or immature stages within any tissue of the trees (Reis et al. 2018).

Oligophagy and avocado crops

Persea americana is a highly attractive and suitable host for Heilipus species, providing food for adults and appropriate tissues for oviposition and larval development. Currently, ten species of Heilipus are associated with avocado in the Americas: three seed borers and seven trunk and branch borers. The biology of the three seed borers was documented in the early 20^th century (Barber 1912, 1919; Dietz and Barber 1920), with H. trifasciatus being the last reported in 1920 (Dietz and Barber 1920). In contrast, the incidence of avocado trunk borers has increased since H. catagraphus was recorded in Brazil by Bondar (1915). Subsequent reports documented H. squamosus in the United States (Wolfenbarger 1948), H. rufipes in Brazil (Lourenção et al. 2003), H. elegans in Colombia (Rubio et al. 2009) and H. albopictus in Mexico (Castañeda-Vildózola et al. 2010). The most recent reports are from Colombia and include H. fassli (first mentioned in this study) and H. leopardus (Díaz-Grisales 2019).

The increasing incidence of Heilipus species on commercial avocado crops can be analysed through interactions between native insects and non-native plants (Bezemer et al. 2014; Sunny et al. 2015; Tallamy et al. 2020). Although Persea americana is native to the Americas, with a natural distribution from Mexico to Peru (Téliz and Marroquín 2019), commercially developed avocado cultivars (e.g. Bertanha, Booth 8, Choquette, Hass, Fortuna, Fuerte, Lorena etc.) may act as non-native plants in regions where they are cultivated. The introduction of non-native plants can alter the landscape for resident arthropods by affecting the regional coverage or abundance of native plant species (Bezemer et al. 2014). The establishment of avocado plantations has led to the replacement of native vegetation in some countries. In Michoacán, Mexico, deforestation and forest fragmentation have accompanied the expansion of avocado crops, illustrating this phenomenon (Cho et al. 2021; Denvir et al. 2022; Saldaña and Cota 2022). In the absence of their native host and being oligophagous, native populations of Heilipus are expected to migrate to a confamilial host. Given its close ecological association with Lauraceae, cultivated avocado is a suitable congener. Moreover, the introduction of non-native plants that serve as a highly suitable host can cause native insects to shift their primary or native host (Bezemer et al. 2014). Avocado monocultures may provide concentrated, high-quality resources for native populations of Heilipus, compared to their native host plants. Consequently, the likelihood of novel interactions between Heilipus species and avocado crops in the Americas depends on the diversity of species confamilial to avocado in the region where it is planted, as well as the diversity of these weevils.

The recent findings of H. fassli and H. leopardus damaging Hass avocado trunks in Colombia are a good example of novel interactions. This damage, recorded over the last five years, coincides with a 105% increase in harvested avocado areas in Colombia, from 53,801 ha in 2018 to 110,183 ha in 2022 (FAO 2023). Three key factors explain the increasing incidence of avocado trunk borers of the genus Heilipus in this country: 1) Colombia is second in Heilipus diversity after Brazil (Díaz-Grisales et al. 2021), 2) it has a significant richness of Lauraceae with 20 genera and 261 species (Soler et al. 2020) and 3) it is one of the top five global avocado producers (Arias et al. 2021; FAO 2023). Colombia’s case is crucial for understanding Heilipus trends in colonising new host plants and ranges. These weevils can even attack non-native Lauraceae plants, as seen with Cinnamomum camphora in Jamaica and Cinnamomum verum in Brazil and Trinidad and Tobago. For avocados, the high specificity of known seed borers (H. lauri, H. pittieri and H. trifasciatus) suggests that other spermophagous Heilipus species are unlikely to target avocado seeds. Instead, generalist species are more likely to infest trunks and branches, as noted by Díaz-Grisales et al. (2021). This aligns with the hypothesis of Tallamy et al. (2020) that insects with larvae feeding on well-defended plant tissues, such as seeds, are less prone to incorporate non-native plants into their diets compared to species whose larval development occurs on less defended tissues, such as wood.

Oligophagy in seed borers

The oligophagous behaviour of spermophagous Heilipus species may have evolved in response to the annual variation in fruit production amongst individuals and species of Lauraceae (Wheelwright 1986). In Los Tuxtlas Biosphere Reserve, Mexico, Damburneya ambigens exhibits cycles of low and high fruit production (Sánchez-Garduño 1995). A seven-year study in Monteverde, Costa Rica, revealed that most Lauraceae fruited abundantly in three non-consecutive years and produced relatively little fruit in the other four years (Wheelwright 1986). In Brazil, irregular fruiting was documented in Aniba rosodora in Manaus, Amazonas (Spironello et al. 2004; Morais et al. 2009). Similarly, Silva et al. (2000) observed irregular flowering and fruiting in Ocotea catharinensis, varying between trees and years in the Parque Estadual da Canta­reira, São Paulo. Heilipus species are likely to colonise other Lauraceae fruits and seeds when their primary or closely-associated host has low or no fruiting periods. This shift may also occur if the primary host has been previously colonised by other more dominant pre-dispersal seed predators. The primary or closely-associated host of Heilipus species remains poorly defined.

The available evidence indicates two levels of specialisation at the generic level in Heilipus: specialist and generalist. Specialists feed on different plant species within the same genus, such as H. albomaculatus on Damburneya seeds and H. lauri and H. pittieri on Persea seeds. Generalists feed on plants from different genera within the family Lauraceae, including H. draco, H. guttiger, H. longirostris, H. vividaensis, Heilipus sp. nov. VDG1 and Heilipus sp. nov. VDG6. Notably, generalists tend to associate with genera from the same clade or lineage within Lauraceae (Table 1). For example, H. albomaculatus, H. draco (with one exception), H. guttiger, H. vividaensis and Heilipus sp. nov. VDG1 specialise in the Cinnamomeae clade, while H. lauri and H. pittieri specialise in the Persea group. This level of specialisation suggests that spermophagous Heilipus species may be evolutionarily predisposed to oviposit in fruits of a specific Lauraceae clade. Genera within the same Lauraceae clade may share Heilipus seed borers due to the similarity in fruit and seed traits important for oviposition.

This tendency to associate with a specific Lauraceae clade is not fulfilled in three cases: Heilipus sp. nov. VDG6, recorded in Aniba sp. (Cinnamomeae clade) and Caryodaphnopsis cogolloi (Caryodaphnopsis group); H. longirostris, associated with Aniba sp. (Cinnamomeae clade) and Mezilaurus sp. (Mezilaurus group); and H. draco, documented on 12 plant species from seven genera, all in the Cinnamomeae clade, except Beilschmiedia tovarensis (Cryptocarya group - Beilschmiedia complex). Data on Heilipus sp. nov. VDG6 and H. longirostris suggest these species have a less common or abundant host belonging to an underrepresented genus in Colombia (Caryodaphnopsis and Mezilaurus) and an alternative host with a wider distribution due to its greater diversity in the country (Aniba). Thus, C. cogolloi and Mezilaurus sp. may be the primary or closely-associated hosts for these Heilipus species, with associations with Aniba sp. occurring during low or no fruiting periods of their main host.

The occurrence of H. draco in B. tovarensis was documented by Downey et al. (2020), who assessed interactions between pre-dispersal insect seed predators and seven Lauraceae species in Barro Colorado Island (Panama) over a two-year period. They concluded that these interactions are not largely related to the phylogenetic distance and trait similarity between hosts, but are likely driven by the volume of fruit produced by each tree species. The relatively high abundance of H. draco on B. tovarensis seeds may be related to fruit availability, as suggested by Downey et al. (2020), but also to the dominance of Pagiocerus frontalis in the other Lauraceae included in the study. The dominance of P. frontalis over another species of the genus Heilipus (H. albomaculatus) was also documented in seeds of Damburneya ambigens in Los Tuxtlas Biosphere Reserve (Rodríguez-Sánchez et al. 2022).

Given these three discussed exceptions, the clade-level specialisation in the spermophagous species of the genus Heilipus must be considered speculative until more data on host plants are available.

With 29 documented species, Brazil records the greatest diversity of the genus Heilipus to date (Clarkson et al. 2024; Sanz-Veiga et al. 2024). Of these, 13 species are found in the southern and south-eastern regions: H. bohemani Boheman, H. catagraphus, H. comtus Boheman, H. crocopelmus Boheman, H. draco, H. gibbus, H. lactarius, H. parvulus, H. peplus, H. rufipes, H. tricolor Perty, H. velamen and H. vividaensis. In the Amazon biome, H. discoides (Fabricius), H. niveodecoratus Lucas and H. odoratus are present. The distribution of H. angusticollis (Pascoe), H. circulatus (Pascoe), H. hopei, H. luctuosus Lucas, H. nudipennis (Pascoe), H. osculatii Guérin and H. paradoxus (Pascoe) in Brazil is uncertain, but they may also occur in the Amazon Region, based on the type localities and material examined from other South American countries. Heilipus rufipes has also been recorded from the central-western and north-eastern regions and H. affinis Guérin from the central-western region. Although H. annuliger (Latreille), H. aulicus (Pascoe), H. empiricus, H. mirus and H. rugicollis Boheman have been reported in Brazil (Wibmer and O’Brien 1986; Clarkson et al. 2024), the specific regions or States of their occurrence remain undocumented.

Brazil also hosts a great diversity of Lauraceae and Annonaceae, with 469 and 389 species, respectively (Flora e Funga do Brasil 2024). With 15 out of 38 records, it is the country with the highest number of reported host plant species for the genus Heilipus in the Americas and the only one where the trunk-boring habit has been recorded in both Annonaceae and Lauraceae. Thirteen of these 15 known host plants, both cultivated and native, are found in the southern and south-eastern regions of Brazil. Ten of them (A. mucosa, A. muricata, A. reticulata, A. sylvatica, O. porosa, O. puberula, N. angustifolia, N. nitidula, O. catharinensis and P. americana) occur in the Atlantic Forest phytogeographic domain (Flora e Funga do Brasil 2024), one of the two biodiversity hotspots in Brazil (Lobão 2017). It is possible that the centre of origin of the genus Heilipus is in the southern and south-eastern regions of Brazil, within the phytogeographic domain of the Atlantic Forest. Two main facts support this hypothesis: 1) nearly half of the Heilipus species recorded in Brazil and more than 60% of their known host plants are found in this phytogeographic domain (Flora e Funga do Brasil 2024) and 2) trunk-boring Heilipus species associated with both Annonaceae and Lauraceae, as well as seed-boring species associated only with Lauraceae, are present in the southern and south-eastern regions of Brazil, in one or more of the phytoecological regions that comprise the Atlantic Forest.