Research Article |
Corresponding author: Zohreh Mirzaee ( zmirzaee1988@gmail.com ) Academic editor: Christian Jürgen Schwarz
© 2023 Zohreh Mirzaee, Saber Sadeghi, Francesco Ballarin, Thomas Schmitt, Marianna Simões, Martin Wiemers.
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:
Mirzaee Z, Sadeghi S, Ballarin F, Schmitt T, Simões M, Wiemers M (2023) Life history and biogeography of the enigmatic mantid Nilomantis floweri (Mantodea, Nanomantidae). ZooKeys 1173: 275-295. https://doi.org/10.3897/zookeys.1173.107204
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The biology and distribution patterns of the Sahelian mantid species Nilomantis floweri are still insufficiently known. For the first time, records are confirmed of this species from Iran and the distribution map of its native range is updated. Records are compiled from the Sahel zone of North Africa, the Arabian Peninsula, and Iran. Detailed information on its biology, oothecal characteristics, male genitalia variation, and intraspecific molecular diversity in the mitochondrial gene cytochrome c oxidase are provided, and ecological niche modelling was used to gain insight into the overall species distribution and understand its climatic niche limits. Genetic analysis revealed only one haplotype shared between Iran and Oman. The Iranian populations likely represent two distinct clusters, both more related to the diverse Oman haplotypes than to each other. Based on new data, N. floweri appears to be mostly associated with coastal areas in southwestern Asia, with the vast majority of records found along the Red Sea, Persian Gulf, and Oman Gulf coasts. This distribution contrasts markedly with N. floweri records in the Sahel, where most collections have been reported in the transitional zone between the southern Sahara and arid thorn savannah, far off the coast. This study contributes to a comprehensive understanding of this still enigmatic mantid species.
Climatic niche, desert species, faunistics, Nilomantini, western Asia
Mantids are a fascinating group of animals and have attracted a lot of attention from scientists and laymen with the consequence of good knowledge about the biology, distribution, and taxonomy of many species (
Known records and the reported number of specimens (NOS) of Nilomantis floweri per country with years of collection, * the collection from 1901 goes back to before the establishment of this genus and species by Werner in 1907. On a trip to Iran, Zarudny collected one male and one female of this species from Makran in Sistan and Baluchistan Province and deposited them at the Zoological Institute of the Russian Academy of Sciences, Saint Petersburg. Evgeny Shcherbakov (Lomonosov Moscow State University, Russia) recently identified them as Nilomantis floweri.
Country | Year | NOS | Reference |
---|---|---|---|
Chad | 1958 | 3 |
|
Eritrea | 1907, 1931 | 3 |
NRM, |
Iran | 1901*–2021 | 35 | This study |
Niger | 1897, 1958 | 4 |
|
Oman | 1976, 2000, 2016, 2017, 2020, 2022 | 45 |
|
Qatar | 2020 | 1 | iNaturalist |
Saudi Arabia | 1930–1932, 1934, 1936, 1938, 1940, 1945, 1948, 1956, 1962, 1975–1980, 2019 | 43 |
|
Sudan | 1906, 1928, 1931, 1957 | 4 |
|
United Arab Emirates | 2014, 2015, 2019–2022 | 18 | iNaturalist |
Yemen | 1987, 1988, 1945, 1956, 1996, 1998, 2000 | 50 |
SMNK, |
External morphology, male genitalia, and geographic distribution have traditionally been used to describe and classify mantid species. Nevertheless, high intraspecific variability in male genital characteristics makes it difficult to separate some closely related species. In addition, intraspecific morphological variability is still unknown or poorly documented for numerous species. In N. floweri for instance, a high variation in the shape of the phalloid apophysis was first pointed out by
Moreover, limited information is available regarding the distributional boundaries of the species. Scattered records are reported in the literature, but lack exact coordinates, and based on its known distribution, sampling gaps are suspected, especially within the African range of the species. In this context, ecological niche models (ENMs) may help to better understand the species’ distribution and shed light on potential sampling gaps.
To fill the knowledge gaps observed in N. floweri, we provide new and updated information on the life history, intraspecific differentiation, and biogeography by providing new data on its distribution, life history traits, ootheca characteristics, morphological variation of male genitalia, and phylogeography. In doing so, we analysed newly collected material from Iran, confirming its presence in this country, and explored the intraspecific morphological and genetic diversity among southwestern Asian populations to improve the general knowledge about this species. In addition, we used ENM to gain insight into its distribution via its climatic niche.
Nine specimens were collected at night by searching the leaves of Conocarpus trees that were planted in urban parks near the sea (Iran: Bandar Bushehr, Bandar-e Lengeh, Kangan, Chahbahar). Six specimens were observed in paddy fields, urban parks, or in mountains with natural springs during day excursions (Firuzabad, Meymand, Jam, Tonbak) (Figs
Female specimens were collected alive in the field and kept in glass jars (15 × 15 × 10 cm) in order to increase the number of available oothecae. These samples were preferentially selected based on their large abdomens assuming that they have previously mated in their natural habitat. Laid oothecae were kept at room temperature (25–27 °C) in separate glass jars (15 × 15 × 10 cm). To simulate their natural dry environment, the relative air humidity (RH) was kept at 50–55% by misting the room on a regular basis. RH was measured using an HTC2 digital terrarium hygrometer (Dongguan, China).
Newly hatched nymphs were housed in separate glass jars (6 × 6 × 4 cm) aiming to obtain information on their life cycle and the number of instars of the species. A woody stick was placed into each jar to help the mantid hang on while moulting. Every three days, they were fed with one to two fruit flies (Drosophila melanogaster Meigen, 1830) or small ants (Trichomyrmex spp.). Living mealworm larvae (Tenebrio molitor Linnaeus, 1758) were fed to later instars twice a week.
Adult specimens were examined under a Leica M205 C stereomicroscope and identified to species level in accordance with
The material used in this study is preserved in the following collections: ESPC (personal collection Evgeny Shcherbakov, Ramenskoye, Russia), SDEI (Senckenberg German Entomological Institute, Müncheberg, Germany),
Distributional data of N. floweri were assembled through fieldwork, museum collections, publications, and online biodiversity databases. In total, 34 records were obtained from various districts of southern Iran over a five-year survey period (2017–2021); 47 occurrences were obtained from museum collections, including the State Museum of Natural History Karlsruhe, Germany (
In total, we obtained 164 occurrence records (Suppl. material
Environmental data were obtained from WorldClim v. 2.0 (http://worldclim.org/version2;
To test the best set of environmental variables, and create the final ecological niche models (ENMs), three environmental sets were used to calibrate our models, based on fieldwork observations by ZM of potentially biologically meaningful variables related to the N. floweri distribution: ‘set 1’, including the maximum temperature of the warmest month (Bio5), minimum temperature of the coldest month (Bio6), annual precipitation (Bio12), precipitation of driest quarter (bio17); ‘set 2’, containing annual mean temperature (Bio1), the maximum temperature of the warmest month (Bio5), annual precipitation (Bio12), precipitation of driest month (Bio14); and ‘set 3’, containing maximum temperature of the warmest month (Bio5), minimum temperature of the coldest month (Bio6), annual precipitation (Bio12), precipitation of driest month (Bio14).
The maximum entropy algorithm in Maxent v. 3.3.3e (
The selected predictors were then used to create final model projections for the current climatic scenario, with ten replicates by bootstrap, logistic outputs, enabling MaxEnt to perform clamping and extrapolation. Binary maps were created from MaxEnt continuous median models using the ten-percentile training presence value as a criterion for viewing and comparing the extent of areas assessed as the possible distribution of N. floweri. The three occurrence data sets were randomly split into training (75% of the data) to calibrate the models, and test (25% of the data) to evaluate the models. All modelling processes were performed using the ‘kuenm’ package (
To evaluate the risk of strict extrapolation, we used the kuenm_mmop function (
Mesocoxal muscle tissue was excised from specimens preserved in 96% ethanol. Total genomic DNA was extracted using the E.N.Z.A Tissue DNA Kit protocol for animal tissue. Amplification of a fragment of the Cytochrome c oxidase subunit I (COI) gene was carried out using the primers LepF1 (5′ATTCAACCAATCATAAAGATATTGG-3′), and LepR1 (5′TAAACTTCTGGATGTCCAAAAAATCA-3′) (
Sequence data were imported into Geneious R10 (https://www.geneious.com) for nucleotide editing and contig assembly. A multiple sequence alignment was performed using Bioedit 7.2.5 (
Individuals of N. floweri were observed resting on the leaves of the tree canopy as well as on grass in grasslands always at some distance from fresh water bodies. They have never been observed on the ground surface. According to our observations, it seems that this species is more active during night. In Iran, it prefers the hot and dry climate of the country’s southern and south-eastern parts. During our observations, two adults in their natural habitat, as well as three adults and two juveniles in captivity, preyed on small ants.
We examined the male genitalia of the specimens that were collected from various districts of Iran’s provinces (four males from Bandar-e Lengeh 27°13'26"N, 56°21'10"E, Hormozgan province; two males from Kangan 27°43'36"N, 52°12'34"E, two males from Jam 27°53'01"N, 52°21'16"E, Bushehr province; one male from Firuzabad 28°53'20"N, 52°33'07"E, Fars province; one male from Chabahar 25°17'40"N, 60°37'17"E, Sistan and Balochistan province). The phalloid apophysis in all specimens showed relatively high variability in shape and length within Iranian populations (Fig.
Male genitalia of Nilomantis floweri and variability of the male apophysis phalloid: a, b Kangan (Iran) c Jam (Iran) d Bandar Lengeh (Iran) e Firooz Abad (Iran) f Chahbahar (Iran) g from right to left; specimens from Mauritania, Niger, Sennaar (Sudan) (type of floweri), Assab (Eritrea) (type of tenella), Eritrea, Jeddah and Mecca (Saudi Arabia). Scale bars: 1 mm (a), 300 µm (b–g). Fig.
The ootheca of N. floweri is ovate (Fig.
Information regarding Nilomantis floweri oothecae. Oothecae one and two were collected from their natural habitat, and three and four were laid in the lab, n = Number.
Ootheca | Width (mm) | Length (mm) | Incubation duration (days) | n eggs | n hatched nymphs |
---|---|---|---|---|---|
1 | 2.3 | 5.0 | 45 | 3 | 3 |
2 | 3.0 | 9.0 | 42 | 8 | 6 |
3 | 2.5 | 7.0 | 42 | 4 | 4 |
4 | 2.2 | 5.5 | 45 | 3 | 1 |
Mean | 2.5 | 6.6 | 43.5 | 4.5 | 3.5 |
SD | 0.4 | 1.8 | 1.7 | 2.4 | 2.1 |
The known native distribution of this species includes tropical deserts, semi-deserts, and thorn savannahs of the Sahel, Arabia, and southern Iran. A total of 206 specimens from 164 locations with different coordinates of N. floweri was examined, with distribution records obtained from countries in North Africa (Mauritania, Niger, Chad, Sudan, and Eritrea), Saudi Arabia, Yemen, Oman, the United Arab Emirates, and Iran (Table
The configurations selected to produce the final model included environmental ‘set 3’, regularisation multiplier 0.5, and linear feature classes (Suppl. material
In addition to the areas where N. floweri has been recorded, our model expands the putatively climatically suitable areas for N. floweri beyond the regions where it has been recorded. This area includes dry and desert regions such as the Gobi Desert in China and Mongolia, the west and south parts of Pakistan, India, Iran’s eastern and central parts, and the northern and southern parts of Africa (Suppl. material
The annual precipitation (Bio12) and minimum temperature of the coldest month (Bio6) had the highest percentage of contribution in predicting the climate niche of N. floweri across its native range, followed by precipitation of the driest month (Bio14) and maximum temperature of the warmest month (Bio5) (Table
Response curves of the most relevant environmental factors affecting the distribution of Nilomantis floweri; the shown values are an average of ten replicate runs a maximum temperature of the warmest month (Bio5) b minimum temperature of the coldest month (Bio6) c annual precipitation (Bio12) d precipitation of driest month (Bio14).
Summary of bioclimatic predictors and their relative importance (in %) to model habitat suitability of Nilomantis floweri across its native range. The pairwise correlation among these layers was less than 0.8.
Abbreviation | Variable | Units | Percent contribution |
---|---|---|---|
Bio 5 | Max temperature of warmest month | °C | 13.2 |
Bio 6 | Minimum temperature of coldest month | °C | 33.6 |
Bio 12 | annual precipitation | mm/a | 38.1 |
Bio 14 | Precipitation of driest month | mm/month | 15.1 |
Our haplotype analysis of the 60 sequences resulted in a single network consisting of 28 distinct haplotypes (Suppl. material
The genus Nilomantis and its type species Nilomantis floweri were described by
In his publication on the Arabian Mantodea,
Despite the high morphological variability that we observed in the shape of the phalloid apophysis (Fig.
Nilomantis floweri represents a unique ecological exception among the Nanomantidae family by preferentially inhabiting arid Sahelian areas. The members of this family are predominantly associated with moist subtropical and tropical regions (
Our knowledge on the ecology, biology, and habitat preferences of N. floweri, and in general of the entire Nanomantidae family, is very limited. Such information is crucial to identify their conservation status and the response to climate change and should be addressed. According to studies on life cycles of some mantid families, the size, quantity, and quality of food consumed by the female can impact the size of the oothecae and the number of eggs per ootheca in mantids (
Our research confirms the presence of N. floweri in Iran and shows that the native range of this species covers all major parts of the Saharo-Arabian realm sensu
Regarding the distribution pattern of N. floweri in Iran and their genetic composition, a natural spreading from the Arabian Peninsula to Iran is plausible. Today, geographic barriers (i.e., the Persian Gulf and the Gulf of Oman) are separating populations of these areas, limiting gene flow between them. On the other hand, these barriers are not constant, allowing exchange among populations, as suggested by their close relationships and the limited number of mutations between their haplotypes. Thus, the Gulf of Oman does not appear as a strong biogeographic barrier for this species since populations living on different sides of the gulf appear directly interconnected by even owing one identical haplotype. Such a close relationship suggests that their separation may have occurred relatively recently or that the current distribution is even the result of human transport. Additionally, the presence of two distinct and genetically distant groups of populations within Iran suggests multiple colonisation events. To further investigate this hypothesis, it is necessary to conduct future studies utilising more comprehensive data, such as increasing the number of samples from populations across its range or employing additional genetic markers. It is highly probable that these events occurred during glacial periods when lower sea levels caused significant desiccation of the Persian Gulf and substantial reduction in the size of the Gulf of Oman (
The climatically suitable areas recovered in our distributional models closely correspond to the known distribution of N. floweri (Fig.
Our final climate niche model (Fig.
MOP analysis (Suppl. material
It is likely that the climatic conditions in southern Africa are suitable for N. floweri, as temperature and precipitation well fall within its required range. However, this area is geographically far away from the present distribution of the species so that absence just might be explained by physical distance. Furthermore, the forests of Central and Eastern Africa, separating Africa’s northern and southern regions (
In addition, species can adapt and evolve over time to overcome barriers and expand their range. Understanding the potential for such adaptations and the mechanisms by which it occurs is an important area of research for predicting and managing species distributions in a changing climate (
Our study sheds new light on the knowledge of this small mantid species, summarising all the published records and reporting new geographic data and information on its ecology based on rearing and newly collected specimens from Iran. Nevertheless, our knowledge of N. floweri is still far from complete. In this regard, the lack of recent records and genetic data for several countries within the supposed range of the species does not allow us to fully understand the distribution and ecology of N. floweri nor its historical biogeography. In particular, the contrasting patterns of distribution and habitat preference in populations from south-western Asia and North Africa remain unresolved. Additional collections in poorly surveyed areas would help to fill these gaps in the future and would also help to determine the conservation status of this Sahelian mantid species.
The authors would like to express their gratitude to the late Roger Roy for his valuable insights and permission to use his drawings of the male genitalia variation in our study. We would like to thank the reviewers and the subject editor for valuable comments and suggestions, which helped us to improve the quality of the manuscript. One of the reviewers also contributed additional data, which we added to the manuscript. We also would like to express our gratitude to Evgeny Shcherbakov (Lomonosov Moscow State University, Russia) and Valeriy Govorov (Charles University, Prague, Czech Republic) for providing the legs of some of the samples from Chahbahar, Sistan, and Baluchistan. We thank Tobias Malm, curator at the Swedish Museum of Natural History, Christoffer Fägerström, curator at the Lund Museum of Zoology (Sweden), and Alexander Riedel, curator at the Staatliches Museum für Naturkunde, Karlsruhe (Germany), for providing coordinates and data on N. floweri. We also wish to thank Hossein Abdollahi and Mohammad Javad Ghasempour for their help during fieldwork.
The authors have declared that no competing interests exist.
No ethical statement was reported.
No funding was reported.
The authors confirm their contribution to the paper as follows: study conception and design: Z. Mirzaee, Saber Sadeghi; data collection: Z. Mirzaee; analysis and interpretation of results: Z. Mirzaee, M. Simões, Francesco Ballarin, Thomas Schmitt, Martin Wiemers; draft manuscript preparation: Zohreh Mirzaee; critical feedback on the manuscript: Saber Sadeghi, Francesco Ballarin, Thomas Schmitt, Marianna Simões, Martin Wiemers. All authors reviewed the results and approved the final version of the manuscript.
Zohreh Mirzaee https://orcid.org/0000-0002-1496-8253
Saber Sadeghi https://orcid.org/0000-0002-3183-8979
Francesco Ballarin https://orcid.org/0000-0003-1417-2519
Thomas Schmitt https://orcid.org/0000-0002-1389-8396
Marianna Simões https://orcid.org/0000-0003-4401-5530
Martin Wiemers https://orcid.org/0000-0001-5272-3903
All of the data that support the findings of this study are available in the main text or Supplementary Information.
New insights into the life history, ecological niche modeling, and biogeography of the enigmatic mantid Nilomantis floweri (Mantodea, Nanomantidae)
Data type: occurences, Modelling data, maps
Explanation note: This document contains maps that display the present climate suitability, accession numbers of samples, information on sample occurrences, and other relevant data utilized in this research. Additionally, it includes data on the performance of 84 different models.