A checklist of Mantodea of Belize, with a regional key to species

Abstract The list of known Mantodea in Belize is updated, with notes of 12 new country records, bringing the total known species of Mantodea in Belize to 21. Further information on habitat and microhabitat observations are included. A regional dichotomous key and Lucid interactive key are provided to known species in Belize. A list of other possibly endemic species is provided. Remarks on the merit of further sampling efforts in central America are made, based on recent studies. Our findings suggest that our understanding of Central American Mantodean diversity could be vastly improved by further documentation.


Introduction
Mantodea, despite being a relatively well-known insect group to the public, has historically received little attention ecologically and taxonomically. Prior to Svenson and Whiting (2004), all the work done on the systematics of Mantodea were based on morphological characters. The study by Svenson and Whiting in 2004 and further (more comprehensively) in 2009, highlighted the rampant paraphyly across the order due to homoplasic traits previously thought to be synapomorphic (Svenson andWhiting 2004, 2009). Recent work by Rivera and Svenson (2016) has significantly improved our current understanding of the order's systematics with the establishment of the Acanthopoidea, the polymorphic earless mantises, along with further clarification of relationships among the Insects were located by sight and collected by hand, in light traps, or in soap traps. Observational microhabitat data was noted when possible for specimens in situ. Preservation and nomenclature follow Brannoch et al. (2017). Systematics follows Schwarz and Roy (2019) for the Cernomantodea, and Rivera and Svenson (2020) for the Acanthopoidea. Specimens were either placed into 95% EtOH or pinned soon after collection. Genitalia were extracted in heated 10% KOH and subsequently preserved (as in Brannoch et al. 2017) for identification and imaging. Photographs taken in the field were taken with an Olympus TG-5 Camera. Figures and diagrams were edited and finalized in GIMP.
Images for the Lucid interactive key were taken via Leica Application Suite and edited in Photoshop. Characters were scored using a Leica M205 C microscope.

Results
We collected over 50 specimens as part of this survey, spanning 14 genera and 19 species. Previously, there were nine recorded species from Belize (Ehrmann 2002;Rivera 2010;Maxwell 2014;Singh 2016a, 2016b;Patel et al. 2016). We have added 12 more species to this list, bringing the total known number of Belizean species to 21. A few taxa, such as Thesprotia Stål, have vague descriptions, and this makes it difficult to identify the nymphs we collected. Morphological characters are still unstable, as thespids undergo significant morphological changes in their post-embryonic development (Svenson and Rivera 2016). We also gathered preliminary information on the microhabitat preference of the mantodean fauna collected, which we note below.
Using the specimens collected we generated a dichotomous key (below) and a Lucid interactive key (http://www.lucidcentral.org). This Lucid interactive key is available at https://keys.lucidcentral.org/keys/v4/mantodea_of_belize/. The aim is to provide both citizens and entomologists unfamiliar with this group with an easy method to identify collected species with high accuracy. Photographs in the Lucid key are included to aid with character determination.

Checklist of the Mantodea of Belize
The following abbreviations are used for the districts of Belize:

CO
Corazal; OW Orange Walk; BD Belize District; CD Cayo District; SC Stann Creek; TD Toledo District.
The following abbreviations will be used for locations in Belize (all locations in Fig. 1 below):

T.E.C.
Tropical Education Center; T.R.E.E.S. Field Station Toucan Ridge Education and Ecology Society Field Station.   Remarks. This species is widely distributed in the Neotropics with records from Brazil to Mexico (Ehrmann 2002). Given records in nearby countries, there are likely other Acontista species in Belize, further sampling is required.

FAMILY ACANTHOPIDAE Burmeister, 1838
Acanthops elegans Lombardo   Remarks. See Fig. 3E. Given the huge range of Choeradodis rhombicollis Latreille in Central and South America, it is more than likely that this species is present in all districts.
Material examined. BZE: Belize Dist.: 4 ♂ collected at light trap, 2 ♂ nymph collected by hand in the vicinity of Tropical Education Center.
Remarks. See Fig. 3F. Females proved difficult to find, given this species' morphology it is likely their behavior is similar to Tarachodes Burmeister or Orthoderella Giglio-Tos, in that individuals prostrate themselves onto a branch or twig.
Remarks. See Fig. 3D. In the rainforest populations, the morphology of the oothecae is greatly modified (Fig. 4). The oothecae are larger, have an air-filled space, and are much darker in color.
Material examined. BZE: Belize Dist.: 2 ♂ collected at light traps in the vicinity of Tropical Education Center.
Remarks. See Fig. 3A. This taxon is a possible synonym of Vates pectinata Saussure (Julio Rivera pers. comm). It is easily distinguished from V. pectinicornis Stål by the small lobe on anterodorsal margin of the forefemora and its presence only in tropical savannah habitat.

Biogeographical remarks
Belize has several types of tropical habitats. The northern states of Belize are lowland tropical savannah and mixed tropical forest, whereas the southern states are at higher elevations, due to the Maya Mountain range. The mountain range passes through parts of the Cayo, Stann Creek, and Toledo districts. These districts are dominated by tropical broadleaf rainforest, regardless of elevation, though urbanization has created other types of habitats. The largest diversity of species, as expected, was found in tropical broadleaf rainforests.
Microhabitat preferences of Mantodea are largely unknown. As a result, though previous studies have mentioned habitats where various taxa have been found (Rivera and Svenson 2016), details such as foliage preference and level (i.e., understory, canopy) are still being ascertained for many species. Noting these findings is important to understanding speciation and life histories of various taxa. For example, Svenson (2014) highlighted the diversity of Liturgusidae in various levels of the rainforest foliage. Such findings necessitate that future studies include further collection details, so more data can be gathered regarding habitat information, and possibly uncover hidden diversity. We include below some observational notes for the genera collected.

Acanthops
Only one species was previously known in Belize, A. godmani (Lombardo and Ippolito 2004;Singh 2016a, 2016b). Given that the species is found in tropical and subtropical habitats, it is no surprise that it was collected in the drier T.E.C. Acanthops elegans was seemingly restricted to tropical broadleaf rainforests and was described from specimens from the tropical rainforests of Guatemala and Costa Rica by Lombardo and Ippolito (2004). One adult female and one nymph were collected at Las Cuevas Field Station, on low hanging tree branches (<3 m off the ground).

Choeradodis rhombicollis
Given that C. rhombicollis is found from the Western Andes to southern Mexico, it seems to be restricted to broadleaf rainforests. Sightings of individuals from tropical mixed forests were reported from T.E.C. by the employees of the site. However, given the confusion of insects by citizen scientists and lack of physical specimens, we do not officially note its presence at this location. This species can be found in Mexico in a few non-rainforest habitats, as recorded in iNaturalist. These individuals tend to be smaller with a less conspicuous pronotum, possibly indicating foliage as a selecting force on morphology. Males were collected at lights from T.R.E.E.S and Las Cuevas Research Station. Individuals were seemingly absent from Bocawina; however, this is likely due to inadequate sampling rather than the species' absence.

Mantoida
This genus is represented by one species. Populations of Mantoida maya showed noticeable variation in size and coloration across the different habitats where they were occurred. In T.E.C., individuals were several millimeters smaller and had a black and white coloration. However, in Las Cuevas, individuals (when alive) were blue as well. It appears that adults may mimic in color pattern and behavior some ichneumonid wasps (see subtribe Mesostenina). The observed variation in size and coloration could be based on selective pressures to better mimic the local wasp species. Mantoida were very common and were found typically on branches 2-3 m above ground at night. Individuals readily flew to lights and headlamps.

Musoniola
Musoniola rapax is the only species in this genus that we collected and included only two adult females and one adult male. The adult male was collected from a light trap low to the ground, but the females were collected on low foliage and on the ground at Las Cuevas Field Station, possibly indicating a lifestyle as forest floor hunting insects.

Phasmomantis
Seemingly only one species of Phasmomantis was collected in Belize, P. sumichrasti. Unexpectedly, P. sumichrasti oothecae displayed morphological differences based on habitat. We were able to confirm the two oothecae were of the same species. From the population at T.E.C., an adult female of P. sumichrasti laid an oothecae in captivity, which we were able to match with wild-collected oothecae. For the population from Las Cuevas Research Station, we were able to find images from Belizean citizen science pages of adult females laying matching oothecae (https://www.facebook.com/ groups/1425989061003132, Creatures of Belize). The wild-collected oothecae both hatched during the trip, and the first instar nymphs were seemingly identical. While first instar morphology is fairly homologous within genera, we feel that the evidence found and examination of genitalia from adult males confirm that these two populations are of the same species.
Phasmomantis sumichrasti did not show much preference for any habitat and was found in tropical broadleaf forest, tropical savannah, and mixed tropical forest. However, all individuals were collected relatively close to the ground (<1.5 m). The differences in oothecae morphology are highlighted below in Figure 4. In the broadleaf forest at Las Cuevas Research Station, oothecae had a hollow space between the outer layer and the eggs, within which we found nesting Camponotus planatus Roger, 1863 in both oothecae collected. Given that C. planatus is a generalist in terms of nest sites, it is possible that the rainforest populations developed this varied structure in response to environmental conditions, and the ants opportunistically took advantage of this space to nest. Unexpectedly, the ants did not consume the eggs. Further research is needed to determine whether this is a type of defensive mutualism, as the ants readily emerged from the oothecae to defend their nest when disturbed.
Only adult males were collected in Las Cuevas Research Station, but these individuals were around 5-10 mm longer than individuals collected in T.E.C. and had a slightly larger eyespot on their hind wings. Males were darker in color. The genitalia examined exhibited only minor morphological differences. The combination of these differences suggests a possible early case of speciation, which will need to be further examined.

Pseudacanthops caelebs
This species' distribution was similar to Choeradodis rhombicollis in Belize. Multiple males were collected at lights in both T.R.E.E.S. and Las Cuevas Field station. Females have not been collected and are undescribed, leaving microhabitat preference unknown for both sexes. Females of other species are noted to hang upside down from mossy branches in the wild (Lombardo et al. 2013). It is not surprising that only males, which are readily found at light traps, were collected. Given the crypsis of this genus, nymphs and adult females are rarely collected, as they are difficult to locate visually and are not attracted to light traps.

Pseudomiopteryx infuscata
Pseudomiopteryx infuscata was commonly encountered and found in nearly every sampled location. Adult females were only collected at T.E.C. and Bocawina, but males were found at all other locations. Most males were perched on or underneath foliage at the edge of the forest at night. It seems elevation does not affect the distribution of the species, as this species has been recorded from multiple locations in Central America at varying elevations and on various types of foliage, indicating the adaptability of this species.  (Saussure, 1861), highlighting the morphological variation in different habitats A tropical savannah, and B tropical broadleaf rainforest. Oothecae from broadleaf rainforests were around twice as large as oothecae from tropical savannah and contained a hollow space between the eggs and outer wall.

Stagmomantis
The genus Stagmomantis shows incredible morphological and ecological diversity (Maxwell 2014), and their distribution in any given habitat is also varied. Stagmomantis fraterna was found frequently at T.E.C. and was found anywhere from 2-5 m above the ground on small shrubs, trees, and other foliage on and under leaves. Stagmomantis carolina was also common at T.E.C. and was found 2-3 m off the ground on various shrubs and trees. Stagmomantis carolina tended to stick more closely to the stems and trunks of the foliage and was found in both T.E.C. and T.R.E.E.S. Stagmomantis heterogamia was collected only at Las Cuevas Field Station, atop large, broadleaf plants, 5-8 m above the ground, and were found only when pulling the plants down to view the tops of the leaves.

Vates
We found both species of Vates at lowland locations. The genus was absent at Las Cuevas Research Station (elev. 650 m), although more sampling will have to be done in order to rule out their presence at higher elevation sites. Almost all individuals were found at lights in T.E.C. and T.R.E.E.S., making it difficult to glean information on microhabitat preference. Vates chopardi was collected in T.E.C., whereas Vates pectinicornis was collected in T.R.E.E.S. Given that V. chopardi is found in Mexico, it appears to be restricted to arid and subtropical zones. Svenson et al. (2016) noted the possible synonymy between V. pectinata and V. chopardi, which is plausible given their overlapping distribution and morphological similarity. Neither of these species has been previously recorded from Belize, however. They are speculated to be a canopy dwelling group (Julio Rivera pers. comm.)

Possible other species
The following are species that have not been found, but possibly occur in Belize, based on records (Ehrmann 2002;Singh 2016a, 2016b;Patel et al. 2016

Conclusion
We expand our knowledge of Belizean mantis fauna by adding 12 new species, bringing the total known species in Belize to 21. The newly found diversity of mantis fauna in Belize highlights the importance to spend more time sampling more countries in Central America to better understand the distribution and diversity of Mantodean fauna. Understanding these distributions can help quantify natural variation as a result of vicariance by distance.
We can also gain valuable information on the ecology of the taxa we found, and how this influences morphology in certain populations. The ability for a species to vary morphologically in different habitats has been demonstrated in several studies in Mantodea (Lombardo and Ippolito 2014;Svenson 2014;Svenson et al. 2016), suggesting that the morphology in Mantodea is highly plastic, and can vary in response to environmental selective pressures.
Given the recent discovery of taxa such as Metacanthops Agudelo &Maldaner, 2019 andHondurantemna Rodrigues et al., 2017 it is not inconceivable that more cryptic and/or monotypic genera remain undiscovered in areas previously sampled. The habitats across Central America vary quite drastically even in the same country, and the presence of several smaller mountain ranges, such as the Maya Mountains, can lead to speciation by allopatry as these ranges can serve as reservoirs or new habitats for existing taxa to colonize, or relicts to persist in.