Research Article |
Corresponding author: Robin Casalla ( casallar@uninorte.edu.co ) Academic editor: Eliana Cancello
© 2016 Robin Casalla, Rudolf H. Scheffrahn, Judith Korb.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Casalla R, Scheffrahn RH, Korb J (2016) Proneotermes macondianus, a new drywood termite from Colombia and expanded distribution of Proneotermes in the Neotropics (Isoptera, Kalotermitidae). ZooKeys 623: 43-60. https://doi.org/10.3897/zookeys.623.9677
|
After more than one hundred years, a new drywood termite of the genus Proneotermes is described from the tropical dry forest in the Caribbean coast of Colombia. Morphological and genetic analyses are given for Proneotermes macondianus sp. n. This termite occurs in tropical dry forests in small colonies inside thin branches of dry wood. The soldier of P. macondianus is smaller and the genal horns are angled outward compared to the other two described Proneotermes species. The imago wings are unusually short and wide. Genetic analyses for COII, 12S, and 16S genes show less than three percent difference between sample localities of P. macondianus. Intergeneric comparison with selected kalotermitid genera indicates that Bifiditermes is the most closely related genus of those sequenced. New morphological descriptions and morphometric measurements of Proneotermes latifrons based on the soldier caste are also included. Neotropical locality records for P. latifrons and Proneotermes perezi are provided.
Northern Colombian coast, Proneotermes keys, Proneotermes macondianus sp. n., tropical dry forest
Colombia’s diverse ecoregions harbour high termite diversity (
For more than a century, the genus Proneotermes was represented by two species, Proneotermes latifrons (Silvestri, 1901) from Venezuela and Proneotermes perezi (
In this paper, a new species of Proneotermes is described, P. macondianus. In addition, new morphological descriptions are included for the soldier of P. latifrons and new soldier measurements provided for P. perezi as well as new locality records for Proneotermes in the Neotropics.
Three study sites in a tropical dry forest near Colombia’s Caribbean coast were selected and surveyed during July 2014 and August 2015 (Fig.
Morphometrics for P. latifrons and P. perezi were obtained from specimens from the University of Florida Termite Collection, Davie, Florida. Specimens of P. macondianus sp. n. were also sequenced for genetic comparisons. Total DNA was extracted from pseudergates and alate imagoes heads using the CTAB protocol (
For the three different haplotypes of P. macondianus from the northern Colombian coast (separated ~200 km from each other), we used the combined COII, 12S, and 16S nucleotide sequences to calculate the p-distance (3000th Bootstrap replications, Gamma Distributed and Transitions + Transversions).
Due to limited availability of mitochondrial gene sequences for Kalotermitidae in National Center for Biotechnology Information (NCBI), we restricted our phylogenetic analysis to only the COII fragment. Twelve genera of Kalotermitidae and Cryptocercus punctulatus as the outgroup were used (Table
Species | Accession COII | GenBank Accession 12S | Accession 16S |
---|---|---|---|
Cryptocercus punctulatus | DQ007637.1 | – | – |
Bifiditermes improbus | AF189079.1 | – | – |
Bifiditermes improbus | AF189080.1 | – | – |
Calcaritermes temnocephalus | EU253877.1 | – | – |
Comatermes perfectus | EU253878.1 | – | – |
Cryptotermes cavifrons | FN377810.1 | – | – |
Cryptotermes longicollis | FN377806.1 | – | – |
Epicalotermes mkuzii | DQ442125.1 | – | – |
Glyptotermes brevicornis | AF189096.1 | – | – |
Glyptotermes iridipenis | AF189096.2 | – | – |
Glyptotermes satsumensis | KP026257.1 | – | – |
Incisitermes immigrans | AB109542.1 | – | – |
Incisitermes tabogae | EU253880.1 | – | – |
Kalotermes flavicollis | DQ442147.1 | – | – |
Marginitermes sp. | KJ907844.1 | – | – |
Neotermes castaneus | HQ215844.1 | – | – |
Neotermes holmgreni | EU253882.1 | – | – |
Neotermes insularis | AF189105.1 | – | – |
Postelectrotermes amplus | DQ442147.1 | – | – |
Postelectrotermes howa | EU253883.1 | – | – |
Procryptotermes leewardensis | EU253884.1 | – | – |
Proneotermes macondianusCE* | KX267096 | KX267094 | KX267091 |
Proneotermes macondianusCO** | KX267097 | KX267093 | KX267090 |
Proneotermes macondianusPT*** | KX267098 | KX267095 | KX267092 |
Specimens were suspended in Hand Sanitizer and images were taken with a Leica MC205 C stereomicroscope coupled to a Leica MC190 HD digital camera. The software Helicon Focus was used to stack pictures. Measurements were done following
Voucher specimens are held at the University of Freiburg, Germany. The holotype soldier and paratypes of Proneotermes macondianus will be deposited at the Natural History Museum of the Alexander von Humboldt Institute of Bogotá (MIAvH) and a paratype soldier at the collection of the American Museum of Natural History, New York. De-alates (wings detached) and pseudergates of P. macondianus will be part of the collection of the Department of Chemistry and Biology at the Universidad del Norte, Barranquilla, Colombia.
The Proneotermes macondianus soldier is smaller and the head capsule lighter than those of P. latifrons and P. perezi. In P. macondianus, the lateral margins of the genal horns angle outward from the sides of the head capsule while, in the other two species, the lateral margins of the genal horns remain in line with the head capsule. The mandibular humps of P. macondianus are more pronounced and rounded than in P. latifrons and P. perezi. Both P. latifrons and P. perezi have more robust rugosity on the frons than P. macondianus. The imago of P. macondianus is smaller and has much shorter, wider, darker, and more punctate wings than that of P. perezi.
Imago (Figs
No. | Measurements in mm (n = 10). | Mean | SD | Range |
---|---|---|---|---|
1 | Head length with labrum | 1.28 | 0.06 | 1.18–1.35 |
2 | Head length to postclypeus | 1.14 | 0.04 | 1.06–1.19 |
3 | Head width, maximum at eyes | 0.95 | 0.04 | 0.88–1.01 |
4 | Eye diameter, maximum | 0.30 | 0.02 | 0.26–0.31 |
5 | Eye to head base, minimum | 0.14 | 0.01 | 0.12–0.16 |
6 | Ocellus diameter | 0.11 | 0.02 | 0.09–0.13 |
7 | Pronotum maximum width | 1.05 | 0.05 | 0.94–1.13 |
8 | Pronotum maximum length | 0.66 | 0.02 | 0.63–0.69 |
9 | Total length without wings | 5.45 | 0.33 | 5.04–5.87 |
10 | Total length with wings (n = 1) | 7.52 | - | - |
11 | Fore wing length to suture (n = 1) | 5.24 | - | - |
12 | Fore wing maximum width (n = 1) | 1.63 | - | - |
13 | No. antennal articulations | 9 | 2.4 | 7–15 |
Soldier (Figs
Soldier heads of Proneotermes macondianus sp. n. (A–C), Proneotermes latifrons (D–F), Proneotermes perezi (G–I). Head in dorsal (A, D, G), lateral (B, E, H) and ventral position (C, F, I). Arrow in 4C denote genal horn projected prominently in Proneotermes macondianus sp. n. Scale bars: 1 mm.
No. | Measurements in mm (n = 11). | Mean | SD | Range |
---|---|---|---|---|
1 | Head length to tip of mandibles | 2.75 | 0.11 | 2.50–2.95 |
2 | Head length to frontal horns | 1.72 | 0.10 | 1.54–1.90 |
3 | Frontal flange width | 1.03 | 0.04 | 0.92–1.08 |
4 | Genal horns outside span | 1.12 | 0.05 | 1.02–1.19 |
5 | Head width max. | 1.23 | 0.06 | 1.14–1.32 |
6 | Head height excluding postmentum | 0.99 | 0.06 | 0.85–1.08 |
7 | Pronotum max. width | 1.19 | 0.07 | 1.05–1.27 |
8 | Pronotum max. length | 0.82 | 0.05 | 0.73–0.87 |
9 | Left mandible length, tip to ventral condyle (n = 1) | 1.10 | - | - |
10 | Total length | 6.57 | 0.44 | 5.43–6.98 |
11 | No. antennal articulations | 11 | 0.7 | 10–12 |
The COII, 12S, and 16S sequences obtained in this study are deposited in GenBank under accession numbers KX267090-KX267098 (Table
Bayesian inference tree, inferred with MRBAYES from COII sequence data (nodes show posterior probability support). Kalotermitidae distribution (X), Species distribution known (O), unknown (?) and established introductions from other regions (I). Neartic = Nea, Neotropic = Neo, Ethiopian = Eth, Paleartic = Pal, Oriental = Ori, Australian = Aus, Papuan = Pap. Distribution based on
Nucleotide distances for combined analysis of COII, 12S rDNA and 16S rDNA genes between localities of P. macondianus sp. n. (p-distance). Standard error estimates are shown above the diagonal.
No. | Species (n = number of sequenced specimens) | Localities | CE | CO | PT |
---|---|---|---|---|---|
1 | Proneotermes macondianus n = 1 | CE | 0.002 | 0.004 | |
2 | Proneotermes macondianus n = 4 | CO | 0.004 | 0.004 | |
3 | Proneotermes macondianus n = 1 | PT | 0.024 | 0.025 |
Nucleotide distances for COII sequences between sample localities P. macondianus sp. n, the cockroach Cryptocercus punctulatus and different Kalotermitidae (p-distance). Standard error estimates are shown above the diagonal.
No. | Specie | 1 | 2 | 3 | 4 | 5 | 6 | 7 | 8 | 9 | 10 | 11 | 12 | 13 | 14 | 15 | 16 |
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
1 | Proneotermes macondianusCE* KX267097 | 0.003 | 0.008 | 0.015 | 0.016 | 0.016 | 0.016 | 0.017 | 0.017 | 0.016 | 0.017 | 0.016 | 0.017 | 0.018 | 0.017 | 0.022 | |
2 | Proneotermes macondianusCO** KX267098 | 0.007 | 0.008 | 0.015 | 0.016 | 0.017 | 0.016 | 0.017 | 0.017 | 0.016 | 0.016 | 0.016 | 0.017 | 0.017 | 0.017 | 0.022 | |
3 | Proneotermes macondianusPT*** KX267096 | 0.040 | 0.044 | 0.016 | 0.016 | 0.016 | 0.016 | 0.017 | 0.017 | 0.017 | 0.017 | 0.017 | 0.017 | 0.017 | 0.017 | 0.021 | |
4 | Bifiditermes improbus AF189080.1 | 0.153 | 0.157 | 0.164 | 0.016 | 0.015 | 0.017 | 0.015 | 0.016 | 0.016 | 0.017 | 0.016 | 0.017 | 0.017 | 0.016 | 0.020 | |
5 | Postelectrotermes howa EU253883.1 | 0.176 | 0.176 | 0.174 | 0.159 | 0.016 | 0.018 | 0.015 | 0.016 | 0.016 | 0.019 | 0.016 | 0.017 | 0.018 | 0.017 | 0.021 | |
6 | Neotermes castaneus HQ215844.1 | 0.184 | 0.179 | 0.177 | 0.165 | 0.157 | 0.017 | 0.016 | 0.017 | 0.017 | 0.018 | 0.016 | 0.018 | 0.017 | 0.016 | 0.022 | |
7 | Incisitermes immigrans AB109542.1 | 0.175 | 0.179 | 0.172 | 0.188 | 0.205 | 0.191 | 0.018 | 0.017 | 0.018 | 0.017 | 0.017 | 0.018 | 0.019 | 0.018 | 0.023 | |
8 | Epicalotermes mkuzii DQ442125.1 | 0.182 | 0.185 | 0.189 | 0.160 | 0.166 | 0.176 | 0.189 | 0.017 | 0.016 | 0.018 | 0.016 | 0.017 | 0.017 | 0.016 | 0.022 | |
9 | Kalotermes flavicollis DQ442147.1 | 0.185 | 0.186 | 0.188 | 0.192 | 0.183 | 0.192 | 0.200 | 0.188 | 0.017 | 0.018 | 0.016 | 0.018 | 0.017 | 0.017 | 0.022 | |
10 | Glyptotermes brevicornis AF189096.1 | 0.187 | 0.187 | 0.197 | 0.185 | 0.184 | 0.197 | 0.214 | 0.196 | 0.200 | 0.018 | 0.017 | 0.018 | 0.016 | 0.018 | 0.022 | |
11 | Cryptotermes cavifrons FN377810.1 | 0.186 | 0.189 | 0.186 | 0.182 | 0.213 | 0.202 | 0.190 | 0.187 | 0.211 | 0.224 | 0.018 | 0.016 | 0.018 | 0.018 | 0.023 | |
12 | Comatermes perfectus EU253878.1 | 0.196 | 0.192 | 0.209 | 0.176 | 0.175 | 0.181 | 0.212 | 0.189 | 0.202 | 0.191 | 0.215 | 0.017 | 0.017 | 0.017 | 0.022 | |
13 | Procryptotermes leewardensis EU253884.1 | 0.199 | 0.199 | 0.189 | 0.194 | 0.176 | 0.187 | 0.189 | 0.194 | 0.202 | 0.219 | 0.160 | 0.204 | 0.018 | 0.019 | 0.022 | |
14 | Calcaritermes temnocephalus EU253877.1 | 0.206 | 0.209 | 0.196 | 0.199 | 0.213 | 0.192 | 0.214 | 0.194 | 0.203 | 0.169 | 0.212 | 0.199 | 0.218 | 0.017 | 0.023 | |
15 | Marginitermes sp. 9MH1 KJ907844.1 | 0.209 | 0.211 | 0.211 | 0.193 | 0.185 | 0.196 | 0.231 | 0.185 | 0.221 | 0.230 | 0.219 | 0.211 | 0.225 | 0.216 | 0.021 | |
16 | Cryptocercus punctulatus DQ007637.1 | 0.282 | 0.282 | 0.279 | 0.254 | 0.255 | 0.281 | 0.291 | 0.261 | 0.266 | 0.267 | 0.280 | 0.266 | 0.279 | 0.290 | 0.257 |
Proneotermes macondianus sp. n was found in tropical dry forests of the Colombian Caribbean near to coastal areas up to 25 km inland (Fig.
Holotype colony: Colombia: Municipality of Santa Marta, Magdalena. Tayrona National Natural Park, Gairaca Bay: 11.3152°N, 74.1032°W (Fig.
Macondianus: In honour of Nobel laureate Gabriel García Marquez and the fictional town “Macondo” in his novel “One hundred years of solitude“. “Macondiano/a” is also a Spanish world used in Colombia to describe an incredible, rare or surprising event that could only be compared with the fictional universe and magical realism of this novel.
Venezuela: Bolivar State, El Pauji: 4.4675°N, 61.5947°W, 600m, 25.VII.2003, J Perozo, University of Florida no. SA336: 2 soldiers and pseudergates. Falcon State, La Chapa: 11.2657°N, 69.6022°W, 703m, 27.V.2008, Scheffrahn et al., VZ833, 2 soldiers, pseudergates. Lara State, Copeyal: 10.4409°N, 69.4402°W, 590m, 28.V.2008, Scheffrahn et al., VZ1014, 10 soldiers, pseudergates. Yaracuy State, Licua: 10.3377°N, 69.1344°W, 650m, 30.V.2008, Scheffrahn et al., VZ1180-11183, 4 colonies, many soldiers, pseudergates.
(Fig.
No. | Measurements in mm (n = 11). | Mean | SD | Range |
---|---|---|---|---|
1 | Head length to tip of mandibles | 2.96 | 0.19 | 2.65–3.35 |
2 | Head length to frontal horns | 1.82 | 0.31 | 1.10–2.25 |
3 | Frontal flange width | 1.06 | 0.12 | 0.90–1.25 |
4 | Genal horns, outside span | 1.33 | 0.12 | 1.20–1.55 |
5 | Head width max. | 1.46 | 0.12 | 1.15–1.60 |
6 | Head height excluding postmentum | 1.17 | 0.14 | 1.00–1.50 |
7 | Pronotum max. width | 1.49 | 0.12 | 1.20–1.65 |
8 | Pronotum max. length | 0.82 | 0.09 | 0.70–0.95 |
9 | Left mandible length, tip to ventral condyle | 1.06 | 0.03 | 1.00–1.10 |
10 | Total length | 7.38 | 0.61 | 6.80–8.80 |
11 | No. antennal articulations | 11 | 0.7 | 10–12 |
Head subsquare with sides slightly convergent, posteriorly and rounded to vertex. Frontal area wide and long, occupies ca 2/5 of head length to postclypeus; narrowly depressed in center, and laterally view with faintly convex and few undulations, sloping angle ca. 50° near to postclypeus. Labrum short and sub-squared. Antennal socket protruded with third antennal segment longer and sclerotized, formula 2<3>4=5=6 and 11 articulations. Postmentum very broad in front. Pronotum as broad as head with anterior emarginated. Mandibles strong and curved inward ca. 45-50°. Measurements are reported in Table
Soldiers of P. latifrons are separated from congeners in having a wide and darker convex frons with narrow undulations dorso-laterally. Postclypeus whitish at border, labrum wider than long and darker postmentum. P. latifrons is distributed in Venezuela, while P. perezi is widely distributed in Central America, from Guatemala to Panama (Fig.
Material examined. Guatemala: San Jose La Arada: 14.6965°N, 89.6255°W, 992m, 3.VI.2006, Scheffrahn et al., GUA768-769, 2 colonies many soldiers, pseudergates3 alates. Ipala: 14.5992°N, 89.6411°W, 873m, 3.VI.2006, Scheffrahn et al., GUA793, 5 pseudergates 6 km NW Jutiapa: 14.3307°N, 89.8622°W, 964m, 3.VI.2006, Scheffrahn et et al., GUA822-824, 3 colonies 3 soldiers, many pseudergates, many alates. San José Acatempa: 14.2537°N, 90.1259°W, 1277m 3.VI.2006, Scheffrahn et al., GUA845-851, 7 colonies many soldiers, pseudergates, 4 alates. Honduras: P. N. Capiro summit: 15.8697°N, 85.9564°W, 942m, 29.V.2007, Scheffrahn et al., HN217, 5 soldiers, many pseudergates. Amarateca: 14.2247°N, 87.3765°W, 991m, 2.VI.2007, Scheffrahn et et al., HN693, 1 soldier, many pseudergates. Panama: Gamboa: 9.12°N, 79.70°W, 9.VI.2005, W. Reeves, University of Florida no. CTA48, 2 alates after rain. Valle de las Minas: 8.6369°N, 82.2114°W, 1050m, Scheffrahn et al., 1.VI.2010, PN1166-1167, 2 colonies many soldiers, pseudergates.
No. | Measurements in mm (n = 10). | Mean | SD | Range |
---|---|---|---|---|
1 | Head length to tip of mandibles | 3.36 | 0.23 | 3.05–3.80 |
2 | Head length to frontal horns | 2.23 | 0.09 | 2.10–2.35 |
3 | Frontal flange width | 0.93 | 0.11 | 0.75–1.10 |
4 | Genal horns outside span | 1.41 | 0.11 | 1.20–1.60 |
5 | Head width max. | 1.52 | 0.09 | 1.30–1.65 |
6 | Head height excluding postmentum | 1.24 | 0.08 | 1.10–1.40 |
7 | Pronotum max. width | 1.46 | 0.13 | 1.20–1.55 |
8 | Pronotum max. length | 0.90 | 0.08 | 0.80–1.00 |
9 | Left mandible length, tip to ventral condyle | 1.28 | 0.08 | 1.15–1.40 |
10 | Total length | 7.88 | 0.60 | 7.00–8.80 |
11 | No. antennal articulations | 12 | 0.9 | 11–14 |
Soldiers with head robust, dark coloration in frons, nearly black, grading from ferruginous orange to orange-yellow toward vertex. Frons sloping between 43–50° to postclypeus, without a ridge and vestigial rugosity. Mandibles bended upwards, with a strong dentition and left mandible bigger than right. Mandibular humps pronounced. Eyes spot unpigmented. Third antennal article larger than second and fourth and sclerotized. Pronotum almost as broad as head width. Femur tick, short and strong. Tibal spurs 3:3:3.
Based on our measurements and morphological description, we developed an identification key for the three Proneotermes species
1 | Smaller species; maximum head width 1.14–1.32 mm (mean 1.23 SD 0.06 mm). Lateral margins of the genal horns angle outward from the sides of the head capsule (Fig. |
P. macondianus sp. n |
– | Larger species; maximum head width1.15-1.65 mm (mean 1.49 SD 0.11 mm); lateral margins of the genal horns remain in line with the head capsule (Figs |
2 |
2 | In lateral view; frons forms even curve below vertex and mandibles (Fig. |
P. latifrons |
– | In lateral view; frons forms rather straight angle from vertex to mandibles (Fig. |
P. perezi |
The phylogenetic relationships within the Kalotermitidae are not clearly resolved yet.
Using a single mitochondrial marker (COII) available for 12 Kalotermitidae genera, our results resemble those from
We thank Universidad del Norte Barranquilla, Colombia, for a research grant to R.C. as part of the Strategic Research Area in Biodiversity, Ecosystem Services and Human Well-being Program, as well as the University of Freiburg, Germany, and COLCIENCIAS-Colfuturo for financial support. We are also grateful to the National Agency of Environmental Licenses for research permit no. 739/ANLA/MADS (8 July 2014) and the Natural Parks Unit research permit 005/PNNC/ANLA/MADS (10 July 2015). Thanks to Miss Sandra Cabarcas for hospitality and the possibility to access the homestead “El Ceibal”, to the field assistants Luis Fernando Lopez and Saudy Royero. Thanks to Karen Meusemann for comments on the text and all those who indirectly helped in conducting this work and the two referees for their constructive comments on the manuscript.