Beta diversity of four braconid subfamilies (Braconidae, Agathidinae, Braconinae, Doryctinae and Macrocentrinae) of the Ria Lagartos Biosphere reserve in Yucatan, Mexico, with some considerations on biological habits
expand article infoRoger Cauich-Kumul, Hugo Delfín-González§, Abdiel Martín-Park|, Pablo Manrique-Saide|, Víctor López-Martínez§
‡ Universidad Tecnológica del Poniente, Maxcanú, Mexico
§ Universidad Autónoma de Yucatán, Mérida, Mexico
| Unidad Colaborativa para Bioensayos Entomológicos, Mérida, Mexico
Open Access


The species diversity composition and phenological behaviour of four braconid subfamilies (Hymenoptera: Braconidae: Agathidinae, Braconinae, Doryctinae and Macrocentrinae) were monitored in three vegetation communities (dune vegetation, tropical deciduous forest and savannah) of the Ria Lagartos Biosphere Reserve (RLBR) in Yucatan, Mexico. Braconid wasps were collected with Malaise traps every 15 days over one year (June 2008 to June 2009). A total of 2,476 specimens were inventoried comprising 233 species and 63 genera. The composition of braconids and their lifestyles differed among the three vegetation communities studied. Doryctinae was the most diverse and abundant subfamily in RLBR (40 genera, 145 species, 990 specimens) and the tropical deciduous forest recorded the maximum abundance and diversity (H’= 4.1; alpha value= 1.059), with 61 exclusive species. Phenological sequence indicates an influence of the rainy season in braconid diversity, but its effects differed among braconid subfamilies and among the vegetation communities. Finally, the importance of the RBRL as a conservation site for this hymenopterous wasp is discussed.


Neotropical, braconid wasps, abundance, conservation


Parasitic Hymenoptera are extremely rich in species of terrestrial ecosystems, especially in tropical areas, and they are a group with a principally parasitoid lifestyle (Noyes 1989, Shaw and Hochberg 2001). Their sensitivity to environmental perturbations makes them good indicators of diversity and environmental stability (Delfín-González and Burgos 2000, Shaw and Hochberg 2001).

Braconidae is the second most diverse family in Parasitic Hymenoptera with about 40,000 species, although its richness is estimated at approximately 100,000 (Hanson and Gauld 2006). Specimens vary in size from 1 to 30 mm. The family is cosmopolitan (Gauld and Bolton 1988, Hanson and Gauld 2006) and members are parasitoids of other insects, mainly Diptera, Coleoptera, Lepidoptera and some Heteroptera (Askew 1971, Gillot 2005). Certain braconid females, called Idiobiont, feed on the host immediately, preventing further development, while others, called Koinobiont, allow the host to continue to reach maturity at a delayed rate. In both types of parasitism, the result is the same: death and potential reduction of future host populations (Quicke 1997). In a few cases, another feeding habit reported in braconids is phytophagy as gall formers (Marsh 1991, Infante et al. 1995, Wharton and Hanson 2005, Penteado-Dias and de Carvalho 2008, Chavarria et al. 2009, Centrella and Shaw 2010, 2013).

Knowledge of the diversity of braconids in Mexico is limited, with only a fraction of the potential species identified (Figueroa-De la Rosa et al. 2003), and few studies characterize the faunal composition of any site (Chay-Hernández et al. 2006, Pérez-Urbina et al. 2011, Ruiz-Guerra et al. 2015). In contrast, the composition and phenology of Braconidae has been documented in several regions of Brazil (Cirelli and Penteado-Dias 2003a, b, Scatolini and Penteado-Dias 2003, Barbieri and Penteado 2012, Souza et al. 2012).

The Ria Lagartos Biosphere Reserve (RLRB) in Yucatán, Mexico, belongs to the Yucatan Peninsula biogeographical province, characterized by areas not exceeding 200 m. altitude with a marine climatic influence. This biogeographic province includes ecosystems that are considered the most threatened globally and have only been the focus of a few faunistic studies (Ramírez-Barahona et al. 2009).

The diversity of Braconidae can be used as an indicator of environmental quality in tropical regions (Delfín-González and Burgos 2000, Barbieri and Penteado 2012), however this has never been evaluated in terms of Neotropical Mexican fauna. This research is the first undertaking of Mexican origin to document the diversity, relative abundance and annual distribution of adult activity of four braconid subfamilies in a region, employing a systematic sampling of three vegetative communities.

Materials and methods

Study area

The Ria Lagartos Biosphere Reserve is in the state of Yucatan, in the Southern Mexico (21°37'29.56"N and 21°23'00.96"N; 88°14'33.35"W and 87°30'50.67"W; 60,347.82 hectares, 100 masl) (Fig. 1). The biosphere is bordered on the north by the Gulf of Mexico; on the south by the municipalities of Tizimin, Rio Lagartos and San Felipe; on the west by the Dzilam State Reserve; and on the east by the Yum Balam Wildlife Protection Area. The climate in most of the reserve is very dry. Temperatures are homogeneous and range between 23 to 27 °C (Arriaga et al. 2002, CONANP 2007, CNA 2006). From June to October, the region receives 62% of the total annual rainfall, with the remaining 38% occuring during the dry season (November to May). The region also experiences between October and February a strong cold northeasterly wind which blows along the shore of the Gulf of Mexico called Norte. (Cuevas-Jiménez and Euán-Ávila 2009). Coastal dune vegetation is integrated with tropical xerophyte species, small and succulent big palms, as Acanthocereus tetragonus (L.), Agave sisalana Perrine, A. vivipara L., Coccoloba uvifera (L.)L., Coccothrinax readii H.J.Quero, Pseudophoenix sargentii H.Wendl. ex Sarg., Opuntia dillenii (Ker Gawl.) Haw., and Thrinax radiata Lodd. Ex Schult. & Schult.f. The dominant plants in the tropical deciduous forest are chandelier-shaped and succulent plants, mainly Cephalocereus gaumeri Britton & Rose, Nopalea gaumeri Britton & Rose, Pterocereus gaumeri (Britton & Rose) Th. acDoug. & Miranda, Stenocereus griseus (Hwa.) Buxb. This type of vegetation is expands from central to eastern areas of Ria Lagartos. Savannah are extensive areas covered with a mixed association of Cladium sp., Phragmites australis (Cav.) Trin. Ex Steud., and Typha sp. (INE 1999, CONANP 2007).

Figure 1. 

Ria Lagartos Biosphere Reserve, Yucatan, Mexico; black dots= savannah sites; black squares= dune sites; white triangles= tropical deciduous forest sites).

Specimen collection

A systematic sampling was taken from the three dominant types of vegetation on the reserve: tropical deciduous forest, savannah and dune vegetation. Cauich-Kumul et al. (2012) describe the ecological and botanical characteristics of each vegetation mentioned above. Among each type of vegetation, two sites were selected, each approximately two hectares in size. Two bidirectional Malaise traps (Townes 1972) were placed in the center of each area to prevent edge effects (Fig. 1). The traps (12 in total) collected samples for 365 days, from June 2008 to June 2009, and the collecting pots were replaced every two weeks (Gonzalez-Moreno and Bordera 2011).

The braconid wasps were stored and handled in accordance with the curatorial standards proposed by Wharton et al. (1998). The taxonomic identification of the specimens was determined using specialized literature (Sharkey 1990, Berta de Fernandez 1998, Marsh 2002, Leathers and Sharkey 2006, Sarmiento-Monroy 2006) and verified by comparisong with specimens held at the Colección Entomológica Regional (CER-UADY) and the Hymenoptera Institute (University of Kentucky). The identified specimens were then deposited at CER-UADY.

Data analysis

Richness was characterized by the number of species found (Moreno and Halffter 2001) and using rarefaction curves (Jiménez-Valverde and Hortal 2003). The Shannon-Wiener index (H’) was used to assess diversity and evenness (E) of the four braconid subfamilies in each vegetation type, based on richness and abundance data (Halffter et al. 2001, Feinsinger 2003). The Solow test (1993) was employed to detect differences in braconid diversity among habitats, using Species Diversity and Richness 3.02 software (Henderson and Seaby 2002). To simultaneously compare patterns of species abundance and diversity among vegetation types, rank-abundance curves (Magurran 1988, Feinsinger 2003) were created. Beta diversity (spatial β) was calculated using the index of complementarity (Price 1984). This index highlights the difference in the species list from two habitats or communities as a percentage, to determine if the replacement of species is linked to factors such as the distance between habitats, vegetation structure or environmental heterogeneity (Colwell and Coddington 1994, Halffter and Moreno 2005, Pineda et al. 2005). Phenological graphs evaluated braconid flight patterns, with reference to the wet (June to August) and dry (March-May) seasons.

Classification of braconid biological host development strategies (koinobiont, idiobiont, phytophage) was followed according to Harvey et al. (2013). Reported information were used for the taxa identified (Shaw and Huddleston 1991, Wharton et al. 1998, Marsh 2002).


Species richness

2,476 specimens of the four subfamilies were collected and classified under 63 genera and 233 species; 77 taxa were determined as morphospecies; 29 of these lack taxonomic keys; 15 are new species (Table 1). The subfamily with the highest number of species and specimens was Doryctinae, 145 and 990, respectively; Agathidinae exhibited the second highest, with 39 species and 942 specimens. The two subfamilies constitute 78.9% of all species and 78% of all specimens collected in the RLBR (Table 1).

Braconidae richness and abundance in the RLBR, Yucatan, Mexico.

Subfamily Generic richness Species richness Abundance
Agathidinae 14 39 942
Braconinae 5 31 222
Doryctinae 40 145 990
Macrocentrinae 4 18 322
Total 63 233 2476

The genus with the highest number of species was Heterospilus (18), followed by Ecphylus (17), Bracon (16), Allorhogas and Macrocentrus (10). Together these genera represented 30.4% of the species collected. The remaining 61 genera were represented by one to seven species. The tropical deciduous forest represented 39.2% of the specimens (168 species). Savannah and dune vegetation presented similar abundance and species richness (761 and 116; 745 and 120, respectively) (Table 2, 3).

Braconidae richness and abundance in three vegetation communities in the RLBR, Yucatan, Mexico.

Plant community Subfamilies Genera Species Specimens
Dune Vegetation 4 42 120 745
Savannah 4 44 116 761
Tropical Deciduous Forest 4 89 168 970

Life strategies and habitats for Braconidae genera collected in Ria Lagartos reserve, Yucatan, Mexico.

Subfamily Genus Host development strategy Habitat
Idiobiont Koinobiont Phytophagous Dune Savannah Tropical deciduous forest
Agathidinae Alabagrus X X X X
Amputoearinus X X
Cremnops X X
Zacremnops X X X
Zelomorpha X X X X
Braconinae Atanycolus X X X X
Bracon X X X X
Compsobraconoides X X X
Digonogastra X X X X
Doryctinae Acrophamus X X X X
Allorhogas X X X X
Caigangia X X X X
Callihormius X X X X
Coiba X X X X
Curtisella X X
Ecphylus X X X X
Glyptocolastes X X X X
Gymnobracon X X
Hansoonorum X X X
Hecabolus X X
Heterospathius X X X
Janzenia X X
Johnsonius X X X
Labania X X
Leluthia X X X X
Masonius X X X
Notiospathius X X X X X
Doryctinae Odontobracon X X X X
Pedinotus X X
Pioscelus X X X
Platydoryctes X X X X
Psenobolus X X X
Rhaconotus X X X X
Spathius X X
Stenocorse X X X X
Macrocentrinae Austrozele X X
Dolichozele X X
Hymenochaoinia X X X X
Macrocentrus X X X X

Rarefaction curves do not reach an asymptote (Fig. 2), indicating that there are many uncollected species. Tropical deciduous forest composition could potentially be more diverse, and dune vegetation and savannah share similar numbers of species.

The tropical deciduous forest had the highest diversity value, according to the Shannon-Wiener index, while the lowest value was collected from savannah vegetation (Table 4). The Solow diversity contrast test (Delta values) demonstrated that the tropical deciduous forest is statistically more diverse than the savannah and dune vegetation; and the dune vegetation is more diverse than the savannah vegetation (α<0.05) (Table 4).

Figure 2. 

Species accumulation and rarefaction curves in three vegetation communities in the Ria Lagartos Biosphere Reserve, Yucatan, Mexico (TDF= Tropical Deciduous Forest, S= Savannah and DV= Dune Vegetation).

Diversity indexes and number of braconid species collected according biological host development strategies and three vegetation communities in the RLBR.

Tropical deciduous forest Savannah Dune vegetation
Shannon-Wienner (H’) 4.1 3.1 3.9
Delta (α < 0.05) 1.059 0.144 0.915
Koinobiont 42 32 29
Idiobiont 115 77 84
Phytophagous 11 7 7

Tropical deciduous forest community

This community was the richest in number of species and had the greatest equality value (Table 2, 3, 4). The most abundant species in this vegetation were: Alabagrus albispina (Cameron), with 139 specimens; Macrocentrus sp8, with 103 individuals; and Heterospilus sp17, with 34 specimens (Fig. 3). Alabagrus albispina and Macrocentrus sp8 provide most of the abundance for this area (10%). The idiobiont strategy predominated, with 115 species, principally Doryctinae. Koinobionts were represented by 42 species. This type of community had the highest number of potential phytophagous species, with 11 species of Allorhogas (Table 3).

Figure 3. 

Braconidae rank/abundance curves in three vegetation communities in the RLBR (only the most abundant species are included). A= Alabagrus albispina, B= Macrocentrus sp8, E= Macrocentrus sp2, S=Macrocentrus sp6, C= Heterospilus sp17, D= Heterospilus sp2, F= Heterospilus sp12, G= Heterospilus sp8, H= Heterospilus sp3, I= Heterospilus sp4, J= Heterospilus sp6, N= Heterospilus sp1, K= Lytopilus sp2; L= Bracon sp4, O= Bracon sp2, M= Zelomorpha arizonensis, P= Zelomoropha lenisterna, Q= Cremnops ferrugineus, R= Cremnops melanoptera, T= Coiba woldai and U= Zacremnops cressoni.

Savannah community

This vegetation type was the least equitable community studied, but the second with highest abundance, with a total of 761 specimens collected. The dominant species were A. albispina, with 340 individuals, followed by Lytopilus sp2, with 22 specimens (Fig. 3). Idiobiont species were more species-rich than koinbionts, with 77 and 32 species, respectively. The number of potential phytophagous species was equal to that one found among dune vegetation (7) (Table 3).

Dune vegetation community

This vegetation community had richness and equity values similar to that of tropical deciduous forest (Table 4), but it was less abundant in specimens (Table 2). The dominant species were Cremnops ferrugineus (Cameron) and Zelomorpha arizonensis Ashmead, which provided the highest abundance recorded for this area, with 134 and 33 specimens, respectively (Fig. 3). The composition of life history strategies was similar to that reported for savannah vegetation, with 29 koinobiont and 84 idiobiont species. The number of potential phytophagous species was also similar to that observed in the savannah (7 species) (Table 3).

Beta diversity (β)

The results obtained through the index of complementarity indicate that the tropical deciduous forest and the savannah had the highest value, with 83% and 77 species shared. The second highest value was for tropical deciduous forest and dune vegetation at 80%, sharing 88 species. Finally, for the savannah and dune vegetation the complementarity index was 69% with 64 shared species (Fig. 4). Overall, the values calculated represent relatively high beta diversity for Braconidae in the RLBR.

Figure 4. 

Exclusive and shared Braconidae (Insecta: Hymenoptera) species in three vegetation communities in the RLBR, Yucatan, Mexico.

Braconidae phenology

Braconidae wasps are active throughout the year, but the number of species and individuals varied across the collection period. 73 species were collected in the rainy season, while 64 were collected during the driest months. June was the month with the highest species richness during the rainy season (66 species), while April exhibited the highest species richness during the dry season (57 species). In November and December (Nortes season), braconid activity was low, with only 34 species collected and a maximum richness reported in November with just 26 species. Amazondoryctes bicolor Barbalho and Penteado-Dias, Coiba woldai Marsh, Hansonorum carolinae Marsh, Odontobracon janzeni Marsh, O. nigra Marsh, O. nigriceps Cameron, Rhaconotus chrysochaitus Marsh and R. rugosus Marsh, were collected throughout the year. Except in the tropical deciduous forest, Agathidinae was abundant in all the vegetation zones, peaking in June (tropical deciduous forest), July (savannah) and August (dune vegetation) (Figure 5). In the tropical deciduous forest, Doryctine abundance peaked in June. Agathidinae was the subfamily least represented in the tropical deciduous forest. Macrocentrinae abundance was highest in the dune vegetation and in the tropical deciduous forest.

Figure 5. 

Phenology of four Braconidae subfamilies (Agathidinae, Braconinae, Doryctinae and Macrocentrinae) in three vegetation communities in the RBRL, Yucatan, Mexico.


The 233-species recorded in this study exceed the diversity and abundance reported by other authors for a single ecosystem; Whitfield and Lewis (1999) mentioned 23 subfamilies, 84 genera and 251 morphospecies in Arkansas, USA; Idris and Hasmawati (2002) reported 19 subfamilies and 95 morphospecies in disturbed Sengalor forests of Malaysia. In Brazil, the number of subfamilies recorded from one locality varies widely, from 10–17 subfamilies, 19–56 genera, but without a clear definition of the species collected (Scatolini and Penteado-Dias 2003, Barbieri and Penteado 2012, Souza et al. 2012). In Mexico, the only comparable study is from Chay-Hernández et al. (2006), who collected 21 subfamilies, 84 genera and 342 species in cultivated areas in Yucatan; and Pérez-Urbina et al. (2011), with 25 subfamilies, 130 genera and 156 species in a locality from Tamaulipas. The latter study showed that braconids exceeded the diversity of its sister group, Ichneumonidae, in the same locality. González-Moreno and Bordera (2012) recorded 148 Ichneumonidae species for the RLBR. Ruiz-Guerra et al. (2015) recorded 65 species and 15 subfamilies in a region of Veracruz. Our results suggest that Yucatan State has the highest number of braconid species and genera in the country.

The greater diversity of braconid wasps reported in this study, as compared to other studies, is most likely a result of using 12 Malaise traps to take samples, which is the best method for catching ichneumonoids (Papp 1999, Fraser et al. 2008). Replicas of sampling sites were also made. Species richness of Ichneumonoidea is underestimated globally, and in Neotropical environments the systematic use of Malaise trapping is increasing our knowledge of its diversity (Sääksjärvi et al. 2004, Cauich-Kumul et al. 2012, González-Moreno and Bordera 2012).

With the results obtained in this work, the community of Braconidae in Yucatan is becoming the most identified in Mexico, in terms of diversity and taxonomic classification, even with many taxa still to describe (López-Martínez et al. 2011, Cauich-Kumul et al. 2014).

Diversity of Braconidae in the three vegetation sites sampled

The braconid subfamily alpha diversity reported here may be the result of plant complexity and the resulting diversity of host availability. Tropical deciduous forests in the Yucatan have up to 103 different species of woody plants in a small area (0.1 hectare) (Gutierrez et al. 2011). By example, a large proportion of palm genera and subfamilies reported from Mexico are in Yucatan tropical deciduous forests (Alvarado-Segura et al. 2012).

In RLBR Doryctinae had the highest abundance and species richness. This is the second most diverse subfamily of Braconidae, with at least 200 genera in the Neotropics (Marsh 2002). In the present study we collected 145 species belonging to 40 genera (Table 1), representing 20.5% of all Neotropical doryctine genera. The subfamily exhibits a broad host range primarily on larval Coleoptera (Bruchidae, Bostrichidae, Buprestidae, Cerambycidae, Curculionidae, Proterrhinidae), but also on Lepidoptera (Brachodidae, Crambidae, Gelechiidae, Phycitidae, Pyralidae and Pyraustidae) (van Achterberg and Shaw 2010), and rarely Symphyta (Xiphydriidae) and Embioptera (Belokobylskij et al. 2004). Phytophagy is another biological habit registered for doryctines (Marsh 1991, Infante et al. 1995, Penteado-Dias and de Carvalho 2008, Chavarria et al. 2009, Centrella and Shaw 2010). This variety of habits provides Doryctinae with numerous possibilities to exploit biological resources in different ecosystems.

In contrast, the low abundance and diversity of Braconinae may be a consequence of the distribution of its subfamily. Although it is cosmopolitan, it is more diverse in the Old-World tropics (Penteado-Dias et al. 2007).

With respect to the diversity between habitats, the greatest similarity occurred in the tropical deciduous forest and dune vegetation communities (88 species in common). We suggest that the low β diversity found in the studied area may be the result of a higher proportion of generalist idiobionts species (Askew and Shaw 1986). The changes in the spatial structure, such as patch types or an increase in patch isolation, could modify the capacity of these organisms to disperse. Likely, the generalist idiobiont species cannot disperse effectively because of a change in structure, suffering decreases in regional population sizes (Fahrig and Merriam 1994). In addition, the three ecosystems have completely different vegetation cover that could impact the species diversity (CONANP 2007).

Life strategies: koinobionts, idiobionts and phytophagous

Molecular evidence suggests that the common ancestor of Ichneumonoidea was a concealed host idiobiont parasitoid (Belshaw and Quicke 2002). Koinobiosis is considered a more derived characteristic than idiobiosis in Braconidae, despite the high percentage of koinobiont species (Wharton 1993, Kasparian 1996). The specialization of the koinobiont species in the subfamilies studied in the RLBR is common and is possibly due to the strong selection pressure which led them to modify and develop certain characteristics to maintain these high abundance levels over time (Thompson 1994).

The idiobiont life strategy (generalists) was consistent among the four subfamilies and in all three types of vegetation studied. It was present in greater abundance in the tropical deciduous forest (49%). In this habitat A. albispina had the greatest number of individuals. The koinobiont life strategy had the highest proportion of species in the tropical deciduous forest (18%) and in the dune vegetation (12%) (Table 3). However, our findings cannot explain the influence of vegetation type on the braconid biological traits distribution. Perhaps, the inclusion of highly diverse koinobiont subfamilies like Microgastrinae, Alysiinae and Opiinae could provide more clarity on this topic. Based on previous works (Owen and Owen 1974, Rathcke and Price 1976, Janzen 1981, Hawkins 1990), koinobionts species richness is lower in the tropics, but richness of generalist idiobiont species exhibit high values. However, Askew and Shaw (1986), Wharton (1993) and Hawkins (1994) argue that idiobionts species are less abundant in the tropics. Chay (1999), Cicero (2002), González (2002), Burgos (2003) and Chay-Hernández et al. (2006), mention that koinobionts species increase according to the degree of habitat disturbance, which can be compared to the study of Restello and Penteado-Dias (2006) in Brazil, where they conclude that braconids are more abundant in areas with some degree of modification.

Phytophagy has been a well-known phenomenon identified in Braconidae since 1989, when Macêdo and Monteiro reported an undetermined species of Allorhogas as a consumer of Leguminosae seeds. Phytophagous braconids primarily produce galls on stems and fruits, from feeding on seeds or fruits, and feed on species of Araceae, Burseraceae, Fabaceae, Melastomataceae, Mimosaceae, Moraceae, Proteaceae, Rubiaceae and Solanaceae. The phytophagic life strategy occurs primarily in the Neotropics, in species of Allorhogas, Bracon, Monitoriella and Psenobolus (Marsh, 1991, Infante et al. 1995, Ramirez and Marsh 1996, Marsh et al. 2000, Marsh 2002, Flores et al. 2005, Centrella and Shaw 2010, Martinez et al. 2011, Perioto et al. 2011, Shimbori et al. 2011, Centrella and Shaw 2013). The number of potential phytophagous species collected in the RLBR are represented in 75% of the genera known with this biological trait and indicate a future need to determine the interactions between host plants and phytophagous braconids, its abundance and its role in the vegetation composition.

Braconidae phenology

The largest number of individuals and species (1050 and 73, respectively) was collected during the rainy season (June-July), a result which correlates with that reported by Falcó et al. (2006); while the lower specimen abundance and species-richness occurred in the dry season (February-March), with 233 individuals and 57 species. Rain favors the profusion of plants and its associated phytophagous and xylophagous insects, which are the potential hosts on which parasitoids depend (Falcó et al. 2006). The rainy season is also when foliage, fruits and seeds provide niches and nutrients for the development of herbivore species.

Our results do not match those reported by González (2002), who concluded that Braconidae communities reach higher abundances in the dry season. Rain is considered a factor that negatively affects the movement of small Hymenoptera species (Speight et al. 1999). Evidently, this was not the case in our study, as similar abundances or small sized species of the four Braconidae subfamilies were collected in both dry and rainy seasons.

The seasonality of koinobiont braconids is determined by the phenology of their hosts (Memmott et al. 1994, Wolda 1988). Idiobionts typically have a wider host range (Sharkey 1993) and are not necessarily synchronized with the life cycle of any one host, but rather by abiotic factors (Memmot et al. 1994). Random patterns might be expected over time.

Ría Lagartos Biosphere Reserve significance

The RLBR is the only nesting site of the pink flamingo (Phoenicopterus ruber L. ruber) in Mexico (Fraga 2006), with a high fish species-richness in the coastal area (Peralta-Meixueiro and Vega-Cendejas 2011) and a growing reported insect richness (González-Moreno and Bordera 2011, 2012, Cauich-Kumul et al. 2014). Cué-Bär et al. (2006) granted the RLBR and other Mexican areas with priority conservation status, based on the unique composition of tree species. Floral richness has a direct impact on the Hymenoptera richness, which has been demonstrated in the sister group of Braconidae, Ichneumonidae (Sääksjärvi et al. 2006).


Ria Lagartos Biosphere Reserves with distinctive vegetation types support a vast diversity of four braconid wasp subfamilies (Agathidinae, Braconinae, Doryctinae, Macrocentrinae) in Yucatan, Mexico. It benefits one of the most diverse and abundant braconid subfamilies, Doryctinae, which recorded 40 genera, 145 species, and 990 specimens. Such abundance of species allows us to hypothesize about the existence of several parasitism relationships and the existence of many unknown hosts.


We are grateful to the project “Conservación de insectos en áreas naturales protegidas: aproximación al valor de las estrategias de manejo de la vegetación en la diversidad de parasitoides de la Reserva de la Biósfera Ría Lagartos, Yucatán, México”, sponsored by Agencia Española de Cooperación Internacional para el Desarrollo (AECID) and coordinated by Santiago Bordera Sanjuan and Hugo Delfín G. To CONACYT program for the Master degree scholarship and Kristen O’Connor for her comments that improved the final versión of the manuscript. Special thanks to Suzanna Shugert for grammar corrections.


  • Alvarado-Segura A, Calvo-Irabién LM, Duno R, Balslev H (2012) Palm species richness, abundance and diversity in the Yucatan Peninsula, in a Neotropical context. Nordic Journal of Botany 30: 613–622.
  • Arriaga L, Espinoza JM, Aguilar C, Martínez E, Gómez L, Loa E (2002) Regiones terrestres prioritarias de México. CONABIO, Mexico City, 609.
  • Askew RR (1971) Parasitic Insects. Heinemann Educational Press, 316 pp.
  • Askew RR, Shaw MR (1986) Parasitoid communities: their size, structure and development. In: Waage J, Greathead D (Eds) Insect Parasitoids. Academic Press, London, 225–264.
  • Barbieri CA, Penteado AM (2012) Braconidae (Hymenoptera) fauna in native, degraded and restoration areas of the Vale do Paraíba, São Paulo state, Brazil. Brazilian Journal of Biology 72: 305–310.
  • Belokobylskij SA, Zaldivar-Riverón A, Quicke DLJ (2004) Phylogeny of the genera of the parasitic wasps subfamily Doryctinae (Hymenoptera: Braconidae) based on morphological evidence. Zoological Journal of the Linnean Society 142: 369–404.
  • Belshaw R, Quicke DL (2002) Robustness of ancestral state estimates: evolution of life history strategy in ichneumonoid parasitoids. Systematic Biolology 51: 450–477.
  • Berta de Fernandez DC (1998) Contribución al conocimiento del género Cremnops Foester, 1862 (Braconidae: Agathidinae) en la región Neotropical. Acta Zoologica Lilloana 44: 231–288.
  • Burgos D (2003) Evaluación de la comunidad de himenópteros parasitoides y las relaciones huésped-parasitoide en una milpa de roza-tumba-quema en el Estado de Yucatán, México. Master Thesis. Universidad Autónoma de Yucatán, Mérida.
  • Cauich-Kumul R, Delfin-Gonzalez H, López-Martínez V, Sharkey MJ (2012) Braconid wasps (Hymenoptera: Braconidae) of Northern Yucatan, Mexico: Subfamilies Agathidinae and Doryctinae (excluding Heterospilus Haliday). Journal of the Kansas Entomological Society 85: 186–205.
  • Cauich-Kumul R, López-Martínez V, García-Ramírez MJ, Delfín-González H, Burgos-Solorio A (2014) Two new species of braconid waps (Hymenoptera: Braconidae: Miracinae: Mirax and Rogadinae: Choreborogas) from Mexico. Florida Entomologist 97: 902–910.
  • Centrella ML, Shaw SR (2010) A new species of phytophagous braconid Allorhogas minimus (Hymenoptera: Braconidae: Doryctinae) reared from fruit gall on Miconia longifolia (Melastomataceae) in Costa Rica. International Journal of Tropical Insect Science 30: 101–107.
  • Centrella ML, Shaw SR (2013) Three new species of gall-associated Allorhogas wasps from Costa Rica (Hymenoptera: Braconidae: Doryctinae). International Journal of Tropical Insect Science 33: 145–152.
  • Chavarria L, Paul H, Paul M, Scott S (2009) A phytophagous braconid, Allorhogas conostegia sp. nov. (Hymenoptera: Braconidae), in the fruits of Conostegia xalapensis (Bonpl.) D. Don (Melastomataceae). Journal of Natural History 43: 2677–2689.
  • Chay HD (1999) Diversidad y abundancia de la comunidad de bracónidos (Hymenoptera: Ichneumonoidea) en cultivos de cucurbitáceas y solanáceas y en una selva baja caducifolia en Yucatán, México. Bachelor thesis. Universidad Autónoma de Yucatán, Mérida.
  • Chay-Hernández DA, Delfín-Gonzalez H, Parra-Tabla V (2006) Ichneumonoidea (Hymenoptera) community diversity in an agricultural environment in the state of Yucatán, Mexico. Environmental Entomology 35: 1286–1297.
  • Cicero L (2002) Estructura y comportamiento estacional de comunidades de Ichneumonidae (Hymenoptera) y su comparación con Braconidae (Hymenoptera) en dos selvas bajas del estado de Yucatán. Bachelor thesis. Universidad Autónoma de Yucatán, Mérida.
  • Cirelli NRK, Penteado-Dias MA (2003a) Análise da riqueza da fauna de Braconidae (Hymenoptera, Ichneumonoidea) em remanescentes naturais da Área de Proteção Ambiental (APA) de Descalvado, SP. Revista Brasileira de Entomologia 47: 89–98.
  • Cirelli NRK, Penteado-Dias MA (2003b) Fenologia dos Braconidae (Hymenoptera, Ichneumonoidea) da Área de Proteção Ambiental (APA) de Descalvado, SP. Revista Brasileira de Entomologia 47: 99–105.
  • Collwell RK, Coddington JA (1994) Estimating terrestrial diversity through extrapolation. Philosophical Transactions of the Royal Society (Series B) 345: 101–118.
  • Comisión Nacional del Agua (CNA) (2006) Jefatura de Proyecto de Aguas Superficiales. Subgerencia Regional Técnica. Gerencia Regional Península de Yucatán. Comisión Nacional del Agua, México, 181 pp.
  • Comisión Nacional de Áreas Naturales Protegidas (CONANP) (2007) Programa de Conservación y Manejo. Reserva de la Biósfera Ría Lagartos. Secretaría de Medio Ambiente y Recursos Naturales, 266 pp.
  • Coronado-Blanco JM, Zaldívar-Riverón A (2014) Biodiversidad de Braconidae (Hymenoptera: Ichneumonoidea) en México. Revista Mexicana de Biodiversidad Supl. 85: 372–378.
  • Cué-Bär EM, Villaseñor JL, Morrone JJ, Ibarra-Manríquez G (2006) Identifying priority areas for conservation in Mexican tropical deciduous forest based on tree species. Interciencia 31: 712–719.
  • Delfín-González H, Burgos D (2000) Los bracónidos (Hymenoptera: Braconidae) como grupo parámetro de biodiversidad en las selvas deciduas del trópico: una discusión acerca de su posible uso. Acta Zoológica Mexicana (nueva serie) 79: 43–56.
  • Falcó GJV, Oltra MT, Moreno J, Pujade-Villar J, Jiménez R (2006) Fenología de los bracónidos (Hymenoptera, Ichneumonoidea, Braconidae) del Pirineo Andorrano. Pirineos 161: 111–132.
  • Feinsinger P (2003) El diseño de estudios de campo para la conservación de la biodiversidad. Editorial FAN 2003: 1–242.
  • Figueroa-De la Rosa JI, Valerio AA, López-Martínez V, Whitfield JB, Sharkey MJ (2003) Two new species of Epsilogaster Whitfield & Mason (Hymenoptera: Braconidae) from Mexico and Costa Rica. Pan Pacific Entomologist 79: 198–206.
  • Flores S, Nassar J, Quicke D (2005) Reproductive phenology and pre-dispersal seed-feeding in Protium tovarense (Burseraceae), with a description of the first known phytophagous “Bracon” species (Hymenoptera: Braconidae: Braconinae). Journal of Natural History 39: 3663–3685.
  • Gauld ID, Bolton B (1988) The Hymenoptera. British Museum (Natural History) and Oxford University Press, 332 pp.
  • Giam X, Scheffers BR, Sodhi NS, Wilcove DS, Ceballos G, Ehrlich PR (2012) Reservoirs of richness: least disturbed tropical forest are centers of undescribed species diversity. Proceedings of the Royal Society B 279: 67–76.
  • Gillott C (2005) Entomology. Springer, 831 pp.
  • González A (2002) Estructura de las comunidades de Braconidae (Hymenoptera: Ichneumonoidea) en una selva baja caducifolia decidua y en una selva baja caducifolia espinosa de Yucatán. Bachelor thesis, Universidad Autónoma de Yucatán, Mérida.
  • González-Moreno A, Bordera S (2011) New records of Ichneumonidae (Hymenoptera: Ichneumonoidea) from Mexico. Zootaxa 2879: 1–21.
  • González-Moreno A, Bordera S (2012) The Ichneumonidae (Hymenoptera: Ichneumonoidea) of Ría Lagartos Biosphere Reserve, Yucatán, Mexico. Zootaxa 3230: 1–51.
  • Gutiérrez C, Ortiz JJ, Flores JS, Zamora-Crescencio P, Domínguez MR, Villegas P (2011) Estructura y composición florística de la selva mediana subcaducifolia de Nohalal-Sudzal Chico, Tekax, Yucatán, México. Foresta Veracruzana 13(1): 7–14.
  • Halffter G, Moreno CE, Pineda EO (2001) Manual para evaluación de la biodiversidad en reservas de la biosfera. CYTED-ORCYT-UNESCO-Sociedad Entomológica Aragonesa, 80 pp.
  • Halffter G, Moreno CE (2005) Sobre diversidad biológica: el significado de las diversidades alfa, beta y gamma. Sociedad Entomológica Aragonesa-CONABIO-grupo Diversitas-CONACYT, 242 pp.
  • Hanson PE, Gauld ID (2006) Hymenoptera de la región neotropical. Memoirs of the American Entomological Institute 77: 1–994.
  • Hawkins BA (1988) Species diversity in the third and fourth trophic levels: patterns and mechanisms. Journal of Animal Ecology 57: 137–162.
  • Hawkins BA (1994) Pattern and process in host-parasitoid interactions. Cambridge University Press, 190 pp.
  • Henderson PA, Seaby RMH (2002) Species diversity and richness III. Versión 3.02. Pisces Conservation, 123 pp.
  • Idris AB, Hasmawati Z (2002) Ecological study of braconid wasps in different logged over forest with special emphasis on the Microgastrinae (Hymenoptera: Braconidae). Pakistan Journal of Biological Science 5: 1255–1258.
  • Infante F, Hanson P, Wharton R (1995) Phytophagy in the genus Monitoriella (Hymenoptera: Braconidae) with description of new species. Annals of the Entomological Society of America 88(4): 406–415.
  • Instituto Nacional de Ecología (INE) (1999) Programa de Manejo Reserva de la Biosfera Ría Lagartos. Instituto Nacional de Ecología, Distrto Federal, 203 pp.
  • Janzen DH (1981) The peak in North American ichneumonid species richness lies between 38° and 42°N. Ecology 62: 532–537.
  • Jiménez-Valverde A, Hortal J (2003) Las curvas de acumulación de especies y la necesidad de evaluar la calidad de los inventarios biológicos. Revista Ibérica de Aracnología 8: 151–161.
  • Kasparian DR (1996) The main trends in evolution of parasitism in Hymenoptera. Entomological Review 76: 1107–1136.
  • Klein AM, Steffan-Dewenter I, Bulhori D, Tscharntke T (2002) Effects of land-use intensity in tropical agroforestry systems on coffee flower-visiting and trap nesting bees and wasps. Conservation Biology 6: 1003–1014.
  • Leathers WJ, Sharkey MJ (2003) Taxonomy and life history of Costa Rican Alabagrus (Hymenoptera: Braconidae), with a key to world species. Contributions in Science 497: 1–82.
  • López-Martínez V, Delfín-Gonzalez H, van Achterberg K, Alia-Tejacal I (2011) A new species of the genus Exasticolus van Achterberg (Hymenoptera: Braconidae: Homolobinae) from Mexico. Studies on Neotropical Fauna and Environment 46: 59–62.
  • Mâcedo MV, Monteiro RF (1989) Seed predation by a braconid wasps, Allorhogas sp. (Hymenoptera). Journal of the New York Entomological Society 97: 358–362.
  • Marsh PM (1991) Description of a phytophagous Doryctine braconid from Brasil (Hymenoptera: Braconidae). Proceedings of the Entomological Society of Washington 93: 92–95.
  • Marsh PM (2002) The Doryctinae of Costa Rica (excluding the genus Heterospilus). Memoirs of the American Entomological Institute 70: 1–229.
  • Marsh PM, De Macêdo MV, Pimental MCP (2000) Descriptions and biological notes on two new phytophagous species of the genus Allorhogas from Brasil (Hymenoptera: Braconidae: Doryctinae). Journal of Hymenoptera Research 9: 292–297.
  • Martínez JJ, Altamirano A, Salvo A (2011) New species of Allorhogas Gahan (Hymenoptera: Braconidae) reared from galls on Lycium cestroides Scltdl. (Solanaceae) in Argentina. Entomological Science 14: 304–308.
  • Memmott J, Godfray HCJ, Gauld ID (1994) The structure of a tropical host-parasitoid community. Journal of Animal Ecology 63: 521–540.
  • Menalled F, Marino CP, Gage S, Landis AD (1999) Does agricultural landscape structure affect parasitism and parasitoid diversity? Ecology Application 9: 634–641.
  • Moreno CE, Halffter G (2001) Spatial and temporal analysis of α, β and γ diversities of bats in a fragmented landscape. Biodiversity and Conservation 10: 367–382.
  • Papp J (1999) Five new Microchelonus species from the Neotropical Region (Hymenoptera:Braconidae:Cheloninae). Annales Historico-Naturales Musei 91: 177–197.
  • Penteado-Dias AM, Barbosa MA, Zarbin PHG (2007) A new species of Cervellus Szépligeti (Hymenoptera, Braconidae, Braconinae) with biological notes. Revista Brasileira de Entomologia 51: 8–11.
  • Penteado-Dias AM, de Carvalho FM (2008) New species of Hymenoptera associated with galls on Calliandra brevipes Benth. (Fabaceae, Mimosoidea) in Brazil. Revista Brasileira de Entomologia 52: 305–310.
  • Peralta-Meixueiro MA, Vega-Cendejas ME (2011) Spatial and temporal structure of fish assemblages in a hyperhaline coastal system: Ría Lagartos, Mexico. Neotropical Icthyology 9: 673–682.
  • Pérez-Urbina B, Coronado-Blanco JM, Correa-Sandoval A, Ruíz-Cancino E, Horta-Vega JV (2011) Diversidad de Braconidae (Hymenoptera: Ichneumonoidea) en el matorral espinoso del Cañón del Novillo, Victoria, Tamaulipas, México. Dugesiana 18: 39–43.
  • Perioto NW, Lara RIR, Ferreira CS, Fernandes DRR, Pedroso EC, Volpe HXL, Nais J, Correa LRB, Viel SR (2011) A new phytophagous Bracon Fabricius (Hymenoptera, Braconidae) associated with Protium ovatum Engl. (Burseraceae) fruits from Brazilian savannah. Zootaxa 3000: 59–65.
  • Petraitis PS, Latham RE, Niesennaum RA (1989) The maintenance of species diversity by disturbance. The Quarterly Review of Biology 64: 693–418.
  • Pineda E, Moreno CE, Escobar F, Halffter G (2005) Frog, bat and dung beetle diversity in the cloud forest and coffee agroecosystems of Veracruz, Mexico. Biological Conservation 19: 400–410.
  • Price PM (1984) Insect Ecology. Wiley, 776 pp.
  • Quicke DLJ (1997) Parasitic Wasps. Chapman and Hill, 470 pp.
  • Rathcke BJ, Price PW (1976) Anomalous diversity of tropical Ichneumonidae parasitoids: a predation hypothesis. American Naturalist 110: 889–902.
  • Ramirez W, Marsh PM (1996) A review of the genus Psenobolus (Hymenoptera: Braconidae) from Costa Rica, an inquiline fig wasp with brachypterous males, with description of two new species. Journal of Hymenoptera Research 5: 64–72.
  • Ramírez-Barahona S, Torres-Miranda A, Palacios-Ríos M, Luna-Vega I (2009) Historical biogeography of the Yucatan Peninsula, Mexico: a perspective from ferns (monilophyta) and lycopods (Lycophyta). Biological Journal of the Linnean Society 98: 775–786.
  • Restello RM, Penteado-Dias MA (2006) Diversidade dos Braconidae (Hymenoptera) da Unidade de Conservação de Teixeira Soares, Marcelino Ramos, RS, com ênfase nos Microgastrinae. Revista Brasileira de Entomología 50: 80–84.
  • Ruiz-Guerra B, López-Acosta JC, Zaldívar-Riverón A, Velázquez-Rosas N (2015) Braconidae (Hymenoptera: Ichneumonoidea) abundance and richness in four types of land use and preserved rain forest in southern Mexico. Revista Mexicana de Biodiversidad 86: 164–171.
  • Sääksjärvi IE, Haataja S, Neuvonen S, Gauld ID, Jussila R, Salo J, Burgos AM (2004) High local species richness of parasitic wasps (Hymenoptera. Ichneumonidae; Pimplinae and Rhysilinae) from the lowland rainforests of Peruvian Amazonia. Ecological Entomology 29: 735–743.
  • Sääksjärvi IE, Ruokolainen K, Tuomisto H, Haataja S, Fine PVA, Cárdenas G, Mesones I, Vargas V (2006) Comparing composition and diversity of parasitoid wasps and plants in an Amazonian rain-forest mosaic. Journal of Tropical Ecology 22: 167–176.
  • Sarmiento-Monroy C (2006) Taxonomic revisión of Zelomorpha Ashmead, 1990 and Hemichoma Enderlein, 1920 (Braconidae: Agathidinae) with a phylogenetic analyses of color patterns. PhD Thesis, University of Kentucky, Kentucky.
  • Scatolini D, Pentado-Dias MA (2003) Análise faunística de Braconidae (Hymenoptera) em três áreas de mata nativa do Estado de Paraná, Brasil. Revista Brasileira de Entomologia 47: 187–195.
  • Sharkey MJ (1990) A revision of Zacremnops Sharkey and Wharton (Hymenoptera: Braconidae: Agathidinae. Proceedings of the Entomological Society of Washington 92: 561–570.
  • Sharkey MJ (1993) Family Braconidae. In: Goulet H, Huber JT (Eds) Hymenoptera of the World: An Identification Guide of Families. Agriculture Canada, Ottawa, 362–395.
  • Shaw MR (1994) Parasitoid host ranges. In: Hawkins BA, Shhehan W (Eds) Parasitoid Community Ecology. Oxford University Press, New York, 111–114.
  • Shaw MR, Huddleston T (1991) Classification and biology of braconid wasps (Hymenoptera: Braconidae). Handbooks for the Identification of British Insects 7: 1–126.
  • Shaw MR, Hochberg ME (2001) The neglect of parasitic Hymenoptera in insect conservation strategies: the British fauna as a prime example. Journal of Insect Conservation 5: 253–263.
  • Shimbori EM, Penteado-Dias AM, Nunes JF (2011) Monitoriella Hedqvist (Hymenoptera: Braconidae: Doryctinae) from Brazil, with descriptions of three new species. Zootaxa 2921: 28–38.
  • Souza S, Penteado-Dias AM, de Almeida A (2012) Diversity of Braconidae (Insecta, Hymenoptera) of the Parque Natural Municipal de Porto Velho, Rondonia, Brazil. Revista Brasileira de Entomologia 56: 468–472.
  • Speight MR, Hunter MD, Watt AD (1999) Ecology of Insects – Concepts and Applications. Blackwell Science, 640 pp.
  • Townes H (1972) A light-weight malaise trap. Entomological News 83: 239–247.
  • van Achterberg C, Shaw MR (2010) Pseudorhaconotus enervatus, a new genus and species from Spain (Hymenoptera: Braconidae: Doryctinae). Zoologische Mededelingen 84: 1–5.
  • Wharton RA, Marsh PM, Sharkey MJ (Eds) (1998) Manual para los Géneros de la familia Braconidae (Hymenoptera) del nuevo mundo. The International Society of Hymenopterist, 447 pp.
  • Wharton RA, Hanson PE (2005) Biology and evolution of braconid gall wasps (Hymenoptera). In: Raman A, Schaefer CW, Withers TM (Eds) Biology, Ecology, and Evolution of Gall-inducing Arthropods. Science Publishers, Enfield, 495–505.
  • Winkler K, Wäckers FL, Kaufman LV, Larraz V, van Lenteren JC (2009) Nectar exploitation by herbivores and their parasitoids is a function of flower species and relative humidity. Biological Control 50: 299–303.