Introduction

Materials and methods

Study area

Specimens belonging to the subfamily Doryctinae were collected in the Chamela biological station (Fig. 1), owned by the Instituto de Biología, Universidad Nacional Autónoma de México (UNAM). This station is located within the Chamela–Cuixmala Biosphere Reserve (CCBR), near the Pacific coast in the state of Jalisco(19°29' N, 105° 02' W). The prevailing climate in the area is tropical sub-humid (mean annual temperature 24.6 °C, annual precipitation 788 mm; García 1988). There is a strong seasonality in the region, with alternating rainy (Jul- Oct) and dry (Nov-Jun) seasons. Altitude ranges from 0 to 500 meters above sea level. The dominant type of vegetation is tropical dry forest, which is characteristic of the Mexican Pacífic coast, though patches of tropical evergreen forest, coastal dune, xeric shrubland and mangrove are also present (Rzedowski 1978, Noguera et al. 2002). The relevance of this area lies in the variety of habitats it supports, as well as in its high endemic component of plants, vertebrates and insects (Noguera et al. 2002).

Figure 1.  

Study area. The Chamela Biological Station (IB-UNAM), located within the Chamela-Cuixmala Biosphere Reserve in the estate of Jalisco, Mexico.

Data resources

Taxon treatment

Analysis

Species boundaries

A total of 961 specimens were collected during the ten field trips, of which 883 COI sequences were generated. Fifteen of these sequences had a length lower than 500 bp and thus did not receive a BIN, though they were included in the analysis. The sequences generated belonged to 289 barcoding species and 30 identified genera, though four barcoding species could not be assigned to any genus (Table 2). Heterospilus Haliday was the most speciose genera with 170 barcoding species, followed by Ecphylus Förster (19 spp.), Allorhogas Gahan (15 spp.) and Callihormius Ashmead (14 spp.). Two species belonging to two additional genera (Doryctinus Roman; Monarea fridae, Belokobyskij et al. 2014 were foundfound in the entomological collection at the CBS, increasing the diversity of doryctine genera and species present in the region to 33 and 289, respectively.

Table 2.

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Doryctine genera and number of barcoding species identified in this study (Total 289).

^* Species identified only based on morphological evidence.

Genera	Barcoding species
Allorhogas Gahan	15
Caenophanes Förster	1
Callihormius Ashmead	14
Coiba Marsh	7
Concurtisella Roman	1
Curtisella Spinola	4
Doryctinus* Roman	1
Ecphylus Förster	19
Ficobolus Martínez, Belokobylskij et Zaldívar-Riverón	1
Glyptocolastes Ashmead	8
Heerz Marsh	2
Heterospathius Barbalho et Penteado-Dias	1
Heterospilus Haliday	170
Iare Barbalho et Penteado-Dias	6
Janzenia Marsh	1
Leluthia Cameron	1
Lissopsius Marsh	2
Masonius Marsh	2
Monarea* Szépligeti	1
Neoheterospilus Belokobylskij	3
Nervellius Roman	1
Notiospathius Matthews et Marsh	5
Odontobracon Cameron	2
Ondigus Braet, Barbalhoa et Van Achterberg	2
Panama Marsh	1
Psenobolus Reinhard	2
Ptesimogaster Marsh	1
Rhaconotus Ruthe	3
Sabinita Belokobylskij, Zaldívar-Riverón et Martínez	1
Spathius Nees	1
Stenocorse Marsh	3
Vanderentiellus Marsh	2
Whitfieldiellus Marsh	1
Unidentifed	4

The reconstructed NJ tree recovered the megadiverse genus Heterospilus as non-monophyletic with respect to Heterospathius and Neotherospilus (Fig. 2). The accumulation curve estimations of species richness (Fig. 3) indicates that the number of species that occur in the region has not been reached.

Figure 2.  

Neighbour-joining tree obtained from BOLD that includes 883 nucleotide sequences belonging to doryctine specimens. The distance model used was the Kimura 2 Parameter, the marker was COI-5P, and the 1st, 2nd and 3rd codon positions were included. The sequences had a lengrh greater than 200bp. See Suppl. material 1.

Figure 3.  

DNA barcoding species accumulation curve for the Doryctinae from the CBS (Suppl. material 1).

Twenty new species and two new genera (Sabinita Belokobylskij, Zaldívar-Riverón et Martínez, Ficobolus Martínez, Belokobylskij et Zaldívar-Riverón) have been described by AZR and collaborators from the doryctine specimens collected for this study (Table 3). An update on Zaldívar-Riverón et al. 2010) generic identification was performed. Specimens assigned to Hansonorum Marsh were transferred to Notiospathius, since the former genus is now considered its junior synonym (De Jesús-Bonilla et al. 2011). Moreover, the specimens assigned in the above study to Barbalhoa Marsh and Platydoryctes Barbalho et Penteado-Dias actually belong to Concurtisella and Callihormius, respectively.

Table 3.

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List of the new species described from specimens collected in this study

SPECIES	REFERENCE
Allorhogas coccolobae Martínez and Zaldívar-Riverón	Martínez and Zaldívar-Riverón 2013
Allorhogas crassifemur Martínez and Zaldívar-Riverón	Martínez and Zaldívar-Riverón 2013
Allorhogas jaliscoensis Martínez and Zaldívar-Riverón	Martínez and Zaldívar-Riverón 2013
Allorhogas marshi Martínez and Zaldívar-Riverón	Martínez and Zaldívar-Riverón 2013
Allorhogas parvus Martínez and Zaldívar-Riverón	Martínez and Zaldívar-Riverón 2013
Allorhogas scotti Martínez and Zaldívar-Riverón	Martínez and Zaldívar-Riverón 2013
Ficobolus jaliscoi Zaldívar-Riverón and Belokobylskij	Martínez and Zaldívar-Riverón 2013, Zaldívar-Riverón et al. 2014
Heerz ecmahla Martínez, Zaldívar-Riverón, Ceccarelli and Shaw	Zaldivar-Riveron et al. 2012
Heerz macrophthalma Martínez, Zaldívar-Riverón, Ceccarelli and Shaw	Zaldivar-Riveron et al. 2012
Iare cheguevarai Martínez, Zaldívar-Riverón and Ceccarelli	Martínez et al. 2010
Iare mexicanus Martínez, Zaldívar-Riverón and Ceccarelli	Martínez et al. 2010
Lissopsius jaliscoensis Zaldívar-Riverón, Martínez, Ceccarelli et Shaw	Zaldivar-Riveron et al. 2012
Lissopsius pacificus Zaldívar-Riverón, Martínez, Ceccarelli et Shaw	Zaldivar-Riveron et al. 2012
Monarea fridae Belokobylskij, Zaldivar-Riveron et Coronado-Blanco	Belokobyskij et al. 2014
Neoheterospilus chamelae Martínez et Zaldívar-Riverón	Martínez and Zaldívar-Riverón 2010
Notiospathius crypticus Reséndiz-Flores, Nunes and Zaldívar-Riverón	Reséndiz-Flores et al. 2014
Notiospathius mariachi Reséndiz-Flores, Nunes and Zaldívar-Riverón	Reséndiz-Flores et al. 2014
Ondigus cuixmalensis Zaldívar-Riverón, Martínez, Ceccarelli and Shaw	Zaldivar-Riveron et al. 2012
Sabinita mexicana Belokobylskij, Zaldívar-Riverón and Martínez	Zaldívar-Riverón et al. 2014
Spathius chamelae Belokobylskij and Zaldívar-Riverón	Belokobylskij and Zaldivar-Riveron 2014

Discussion

Acknowledgements

References

Aguilar-Velasco RG (2013)
Diversidad de especies y asociación de parasitoidismo en las avispas de la subfamilia Rogadinae (Hymenoptera: Braconidae) de la Estación de Biología de Chamela, Jalisco. BSc Thesis. Facultad de Ciencias
.
Universidad Nacional Autónoma de México
,
D.F
,
67
pp.
Belokobylskij S (1992)
On the classification and phylogeny of the Braconid wasps subfamilies Doryctinae and Exothecinae (Hymenoptera, Braconidae). Part I. On the classification, 1
.
Entomologicheskoe Obozrenie
71
:
900
‑
928
.
Belokobylskij S, Zaldivar-Riveron A (2014)
The genus Spathius Nees (Hymenoptera, Braconidae, Doryctinae) in Mexico: occurrence of a highly diverse Old World taxon in the Neotropics
.
ZooKeys
427
:
59
‑
73
. https://doi.org/10.3897/zookeys.427.8074
Belokobylskij SA, Zaldívar-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
(
3
):
369
‑
404
. https://doi.org/10.1111/j.1096-3642.2004.00133.x
Belokobyskij SA, Zaldívar-Riverón A, Coronado-Blanco JM (2014)
Phylogenetic affinities of Monarea Szépligeti, 1904 (Hymenoptera: Braconidae, Doryctinae, with description of a new species from Mexico
.
Zootaxa
3795
(
4
):
421
. https://doi.org/10.11646/zootaxa.3795.4.2
Ceballos G, Martínez L, García A, Espinoza E, Bezaury-Creel J, Dirzo R (2010)
Diversidad, amenazas y áreas prioritarias para la conservación de las Selvas Secas del Pacífico de México
.
Fondo de Cultura Económica and Comisión Nacional para el Conocimiento y Uso de la Biodiversidad
,
México, D.F.
,
596
pp. [ISBN
970-9000-38-1
]
Coronado-Blanco JM, Zaldívar-Riverón A (2014)
Biodiversidad de Braconidae (Hymenoptera: Ichneumonoidea) en México
.
Revista Mexicana de Biodiversidad
85
:
S372
‑
S378
. https://doi.org/10.7550/rmb.32000
De Jesús-Bonilla VS, Nunes J, Penteado-Días A, Csösz S, Zaldívar-Riverón A (2011)
A new synonym of the Neotropical parasitoid wasp genus Notiospathius (Braconidae, Doryctinae), with redescription of two species and description of five new species from Brazil
.
ZooKeys
122
:
71
‑
90
. https://doi.org/10.3897/zookeys.122.1243
Fernández-Flores S, Fernández-Triana JL, Martínez JJ, Zaldívar-Riverón A (2013)
DNA barcoding species inventory of Microgastrinae wasps (Hymenoptera, Braconidae) from a Mexican tropical dry forest
.
Molecular Ecology Resources
13
:
1146
‑
1150
. https://doi.org/10.1111/1755-0998.12102
Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994)
DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates.
Molecular Marine Biology and Biotechnology
3
:
294
‑
299
.
García E (1988)
Modificaciones al sistema de classificación climática de Köppen
.
UNAM
,
México, D.F
,
217
pp.
Hawkins B, Hochberg M (1994) The implications of population dynamics theory to parasitoids diversity and biological control. In: Hawkins B, Sheehan W (Eds)
Parasitoid community ecology
.
Oxford University Press Oxford
,
20
pp.
Hebert P, Gregory TR (2005)
The Promise of DNA Barcoding for Taxonomy
.
Systematic Biology
54
(
5
):
852
‑
859
. https://doi.org/10.1080/10635150500354886
Hebert PDN, Ratnasingham S, deWaard JR (2003a)
Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species.
Proceedings. Biological sciences / The Royal Society
270
:
96
‑
9
. https://doi.org/10.1098/rsbl.2003.0025
Hebert PDN, Cywinska A, Ball SL, deWaard JR (2003b)
Biological identifications through DNA barcodes
.
Proceedings of the Royal Society B: Biological Sciences
270
(
1512
):
313
‑
321
. https://doi.org/10.1098/rspb.2002.2218
Jones O, Purvis A, Baumgart E, Quicke D (2009)
Using taxonomic revision data to estimate the geographic and taxonomic distribution of undescribed species richness in the Braconidae (Hymenoptera: Ichneumonoidea)
.
Insect Conservation and Diversity
2
(
3
):
204
‑
212
. https://doi.org/10.1111/j.1752-4598.2009.00057.x
Kimura M (1980)
A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences
.
Journal of Molecular Evolution
16
(
2
):
111
‑
120
. https://doi.org/10.1007/bf01731581
LaSalle J, Gauld ID (1993)
Hymenoptera and biodiversity
.
CAB International
,
Wallingford
,
348
pp. [ISBN
085198830X
]
Marshall S (1994)
Terrestrial Arthropod Biodiversity: Planning a Study and Recommended Sampling Techniques: a Brief
.
Entomological Society of Canada Bulletin
26
(
1
):
1
‑
33
. https://doi.org/10.4039/entm126169fv
Marsh P (2002)
The Doryctinae of Costa Rica (excluding the genus Heterospilus).
Memoirs of the American Entomological Institute
70
:
1
‑
319
.
Marsh P, Wild A, Whitfield J (2013)
The Doryctinae (Braconidae) of Costa Rica: genera and species of the tribe Heterospilini
.
ZooKeys
347
:
1
‑
474
. https://doi.org/10.3897/zookeys.347.6002
Marsh PM (1997) Doryctinae. In: Wharton RA, Marsh PM, Sharkey MJ (Eds)
Manual of the New World genera of the Family Braconidae (Hymenoptera)
.
International Society of Hymenopterists
,
Washington, D.C
,
438
pp.
Martínez J, Zaldívar-Riverón A (2010)
A new species of Neoheterospilus (Hymenoptera: Braconidae: Doryctinae) from Chamela, Jalisco, Mexico
.
Journal of Hymenoptera Research
19
:
217
‑
222
.
Martínez JJ, Zaldívar-Riverón A (2013)
Seven new species of Allorhogas (Hymenoptera: Braconidae: Doryctinae) from Mexico
.
Revista Mexicana de Biodiversidad
84
(
1
):
117
‑
139
. https://doi.org/10.7550/rmb.31955
Martínez JJ, Ceccarelli FS, Zaldívar-Riverón A (2010)
The genus Iare Barbalho and Penteado-Dias (Hymenoptera: Braconidae: Doryctinae) in Mexico, with the description of two new species
.
Zootaxa
2685
:
30
‑
38
.
Noguera F, Vega J, García A, Quesada M (2002)
Historia natural de Chamela
.
Instituto de Biología, UNAM
,
México, D.F
,
xv-xxi
pp. [ISBN
9703205208
]
Ratnasingham S, Hebert PN (2013)
A DNA-Based Registry for All Animal Species: The Barcode Index Number (BIN) System
.
PLoS ONE
8
(
7
):
e66213
. https://doi.org/10.1371/journal.pone.0066213
Reséndiz-Flores A, Nunes J, García-París M, Zaldívar-Riverón A (2014)
Six new species of the parasitoid wasp genus Notiospathius (Hymenoptera: Braconidae: Doryctinae) from Mexico
.
Revista Mexicana de Biodiversidad
85
(
2
):
391
‑
401
. https://doi.org/10.7550/rmb.41972
Rzedowski J (1978)
Vegetación de México
.
Limusa
,
México, D.F
,
432
pp.
Smith MA, Rodriguez JJ, Whitfield JB, Deans AR, Janzen DH, Hallwachs W, Hebert PDN (2008)
Extreme diversity of tropical parasitoid wasps exposed by iterative integration of natural history, DNA barcoding, morphology, and collections
.
Proceedings of the National Academy of Sciences
105
(
34
):
12359
‑
12364
. https://doi.org/10.1073/pnas.0805319105
Wharton R, Marsh P, Sharkey M (1997)
Manual of the New World genera of the family Braconidae (Hymenoptera)
.
International Society of Hymenopterists
,
Washington, D.C
.
Wild A, Marsh P, Whitfield J (2013)
Fast-Evolving Homoplastic Traits Are Best for Species Identification in a Group of Neotropical Wasps
.
PLoS ONE
8
(
9
):
e74837
. https://doi.org/10.1371/journal.pone.0074837
Yu D, van Achterberg C, Horstmann K (2012)
Taxapad 2012, Ichneumonoidea 2011. Database on flash-drive. www.taxapad.com. Ottawa, Ontario, Canada
.
Zaldivar-Riveron A, Martínez J, Ceccarelli F, Shaw S (2012)
Five new species of the genera Heerz Marsh, Lissopsius Marsh and Ondigus Braet, Barbalho and van Achterberg (Braconidae, Doryctinae) from the Chamela-Cuixmala biosphere reserve in Jalisco, Mexico
.
ZooKeys
164
:
1
‑
23
. https://doi.org/10.3897/zookeys.164.2201
Zaldívar-Riverón A, Martínez J, Belokobylkij S, Pedraza-Lara C, Shaw S, Hanson P, Varela-Hernández F (2014)
Systematics and evolution of gall formation in the plant-associated genera of the wasp subfamily Doryctinae (Hymenoptera: Braconidae)
.
Systematic Entomology
39
(
4
):
633
‑
659
. https://doi.org/10.1111/syen.12078
Zaldívar-Riverón A, Martínez JJ, Ceccarelli FS, De Jesús-Bonilla VS, Rodríguez-Pérez AC, Reséndiz-Flores A, Smith MA (2010)
DNA barcoding a highly diverse group of parasitoid wasps (Braconidae: Doryctinae) from a Mexican nature reserve
.
Mitochondrial DNA
21
:
18
‑
23
. https://doi.org/10.3109/19401736.2010.523701
Zaragoza-Caballero S, Noguera F, González-Soriano E, Ramírez-García E, Rodríguez-Palafox A (2010) Insectos. In: Ceballos G, Martínez L, García A, Espinosa E, Bezaury-Creel J, Dirzo R (Eds)
Diversidad, amenazas y áreas prioritarias para la conservación de las selvas secas del Pacífico de México
.
Fondo de Cultura Económica and Comisión Nacional para el Conocimiento y Uso de la Biodiversidad
,
México, D.F
,
596
pp. [ISBN
970-9000-38-1
].