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Article

Termite (Blattodea: Isoptera) Distribution Along an Elevational Gradient in Northwestern African Mountains

by
Aya Najjari
1,
David Hernández-Teixidor
2,*,
Bilal El Ajjouri
1,
Yousra Benyahia
1 and
Ahmed Taheri
1
1
Laboratory of Plant Biotechnology, Ecology and Ecosystem Valorization, Faculty of Sciences of El Jadida, Chouaib Doukkali University, P.O. Box 20, El Jadida 24000, Morocco
2
Island Ecology and Evolution Research Group, Instituto de Productos Naturales y Agrobiología (IPNA-CSIC), 38206 San Cristobal de La Laguna, Canary Islands, Spain
*
Author to whom correspondence should be addressed.
Diversity 2024, 16(12), 714; https://doi.org/10.3390/d16120714
Submission received: 14 October 2024 / Revised: 11 November 2024 / Accepted: 15 November 2024 / Published: 22 November 2024
(This article belongs to the Special Issue Diversity and Ecology of Termites)
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Abstract

:
We examined the distribution of termites along an elevational gradient in the western Rif Mountains of northern Morocco. Sampling followed standardized protocols at nine forest sites (125, 325, 488, 715, 850, 1150, 1316, 1544, and 1700 masl), all except the lowest site within the Intercontinental Mediterranean Biosphere Reserve. We found a total of three termite species, with Reticulitermes grassei (Rhinotermitidae) being the most abundant, followed by Kalotermes flavicollis (Kalotermitinae) and Amitermes sp. (Terminidae). Comparing microhabitat preferences, we found R. grassei and Amitermes sp. exclusively in buried wood and under rocks, and K. flavicollis exclusively in dead tree trunks and surface wood. The findings reveal the distribution of microhabitats along an elevation gradient and the corresponding preferences of termite species across these microhabitats. We found that total termite density decreased significantly with elevation (rs = −0.40; p < 0.001), but with distinct differences among species. Kalotermes flavicollis and Amitermes sp. showed a strong negative correlation between density and elevation. In contrast, for R. grassei, the most common termite, we found no significant correlation. Termite density also varied among forest types, with a non-significant trend (p = 0.075) of higher density in the cork oak forest (hits/m2 = 0.06) compared to holm oak (0.04) and fir–cedar (0.02) forests. This research contributes to the limited knowledge of termite diversity and ecology in northern Africa and western Mediterranean forests.

1. Introduction

Termites play a vital role in the dynamics of tropical ecosystems [1] and are valuable “bioindicators” of habitat disturbances [2]. As detritivores, termites help in the decomposition process by breaking down organic matter [3]. This decomposition activity is crucial for nutrient cycling and the recycling of organic materials in the ecosystem [4,5,6]. In addition, termites significantly impact the soil’s physicochemical characteristics [7]. Some termites have the capacity to amass significant concentrations of various heavy metals [8]. Moreover, they contribute to food networks within the ecosystem [9].
Many termite species remain undescribed, especially in tropical and subtropical regions [10]. In all North Africa, only 17 termite species are known, including only 7 in Morocco [11,12,13]. The ecology of North African termites remain largely unstudied, except for the genus Reticulitermes, which has been the subject of research using molecular markers to uncover the evolutionary history of R. grassei [14,15]. Additional research on the diversity, distribution, and ecological roles of termites in North Africa and the Mediterranean basin is needed to enhance our understanding of the ecosystem dynamics in this region.
Environmental variations influence the distribution of termites. In general, termite diversity decreases when elevation increases [16]. Many studies revealed a negative correlation between elevation and the abundance of termites [17,18,19,20,21,22]. Additionally, the sensitivity of termite populations to differences in elevation, underscoring the importance of considering elevation as a key factor in understanding and predicting termite species composition [23].
In this study, we surveyed termites in the Western Rif region of Morocco to examine how termite diversity and population density vary along an elevational gradient.

2. Materials and Methods

2.1. Study Sites

In May and June 2023, we surveyed termites at nine sites in northern Morocco, eight of which are within the Intercontinental Mediterranean Biosphere Reserve, a vast area spanning ~1,000,000 hectares in Spain and Morocco (IMBR; Figure 1). The IMBR was the first Intercontinental Reserve to be approved by UNESCO in October 2006 [24]. The Moroccan portion of this reserve boasts the presence of an exceptional biodiversity hotspot, the Talassemtane National Park (TLSNP). This protected area encompasses renowned natural landscapes and provides a great variety of habitats for a wide range of plants and animals. The study area stands out as the most humid zone in North Africa [25] This characteristic contributes to the unique ecological conditions and biodiversity found within the reserve. Sampling was carried out at nine sites, ranging from 125 to 1700 m. According to the Koppen–Geiger climate map [26], the climate at the study sites is classified as hot-summer Mediterranean climate (Csa). The sites follow an increasing gradient of temperature and precipitation. The lowest recording station (Tangier) records an average annual temperature of 17.5 °C and average annual precipitation of 574 mm. However, the highest station (Bab Taza) displays an average annual temperature 14.9 °C and average annual precipitation of 1035 mm [27].
Our survey sites spanned an elevation range of 125 to 1700 masl (Table 1). The lower six sites are forests of Quercus suber L. (cork oak) with a thick, tall understory of Erica arborea L., Cistus crispus L., Cistus monspeliensis L., and Arbutus unedo L. The higher elevational sites were forest dominated by Q. ilex L. (holm oak) (1316 m), Abies marocana Trab. (fir) (1544 m), and Cedrus atlantica (Endl.) Manetti ex. Carrière (cedar) (1700 m).

2.2. Sampling

Termites were sampled through an active sampling protocol, with some modifications [28]. The method used employs 50 × 5 m transects divided into ten segments of 5 × 5 m deployed at each site. In each section, we spent one hour examining each section (30 min each for two workers) in four microhabitats: (a) surface soil (under rocks), (b) dry dead wood (trunks and branches on the ground surface), (c) dead trunk fixed to the ground and d) buried dead wood (with galleries in wood in the ground) (Figure 2). The number of encounters with termites (hits) along a transect was used as a measure of the relative abundance of species in each transect.
Specimens of all castes were collected when it was possible. All termites were stored in absolute ethanol and transported to the laboratory for identification and collection.

2.3. Termite Identification

Species identification was carried out at the laboratory LB2VE of the Faculty of Sciences of El Jadida (Morocco). Samples were observed and identified at a specific level under the stereomicroscope magnifying glass Nikon SMZ 745. Termites with soldiers were identified to the genus level using the key to the extant families of Isoptera [12], and to the species level with the key provided by [29].

2.4. Statistical Analysis

All statistical tests were conducted in RStudio version 4.4.0. The average density of termite hits was calculated for both the overall species and for each species. This allowed for the analysis of variations in termite density at different elevation levels. To explore the relationship between termite hit density and elevation, the Spearman correlation method was applied. This non-parametric analysis helped to identify the trends and associations between these two variables, thus understanding whether elevation influences termite density. A correspondence analysis was conducted to examine the relationships between the various termite microhabitats and elevations. This analysis determines how the distribution of microhabitats varies with elevation and how this might affect the presence and density of termites. Finally, the association between termite species and microhabitats was evaluated using a Chi-squared test. This statistical analysis allows for the detection of possible microhabitat preferences among the different studied termite species.
To investigate the correlation between termite density and forest type, we calculated the average termite density in four surveyed forest types: QS: Q. suber; QI: Q. ilex; AM: A. marocana; and CA: C. atlantica. The results were expressed as mean ± standard error mean (SEM). Subsequently, an analysis of variance (ANOVA) was conducted to examine potential differences in density across these forests. p < 0.05 was considered a significant difference. Additionally, a boxplot analysis was performed to visually represent the variability of termite density by forest type.

3. Results

During the sampling period, we found termites belonging to three families, namely Kalotermitidae, Rhinotermitidae, and Termitidae. Each of these families was represented by a single species (Figure 3): Kalotermes flavicollis (Fabricius, 1793) (Kalotermitinae), Reticulitermes grassei Clément, 1978 (Heterotermitinae), and Amitermes sp. (Termitinae), respectively. Reticulitermes grassei was found at all elevations with the highest relative abundance (52.21%), followed by K. flavicollis (38.05%). Kalotermes flavicollis was collected at the three lowest elevations (125, 325, and 488 m) and also at 1150 m. Amitermes sp. exhibited the lowest relative abundance at 9.73%, and was exclusively detected at the first two lowest elevations of 125 and 325 m.
The mean density of hits in the 90 surveyed squares was 0.05 ± 0.006 hits/m2, with a maximum of 0.28 hits/m2 detected in the cork oak forest of Hjar Nhal at an elevation of 125 m (Site 1). This elevation level also shows the maximum density at 0.012 hits/m2 (Supplementary Material, Table S1). After the first elevation, there is a decrease in density, ranging from 0.11 to 0.04 hits/m2. Beyond 488 m, densities appear to remain relatively low, mainly varying between 0.02 and 0.06 hits/m2. However, a slight increase in hits was observed after 1000 m and a posterior decrease after 1150 m (Figure 4A). The linear regression reveals a significant decrease in termite density with elevation, with a coefficient of −4.944 × 10−5 per meter (p = 0.031), explaining 50.77% of the observed variability (r2 = 0.51). This trend underscores the notable impact of elevation on termite distribution.
Kalotermes flavicollis and Amitermes sp. showed strong negative correlation between density and elevation; in contrast, for R. grassei, we found no significant correlation.
Regarding the forest microhabitats where termites were located (Figure 5), buried dead wood (damp and soft wood; BW) represented 36.28% of all hits, dead trunks fixed to the ground (often felled; DT) represented 27.43%, dry dead wood (trunks and branches on the ground surface; DW) represented 10.62%, and under rock (UR) represented 25.66% (Supplementary Material, Table S2). The distribution of termite microhabitats varied according to elevation (Figure 5).
A statistically significant association between elevation and microhabitat types (χ2 = 0.6638; p = 2.09 × 10−9) was detected, indicating that elevation may be a factor influencing the distribution of various termite microhabitats and, consequently, their presence and abundance.
The correspondence analysis (Figure 6) revealed that microhabitats DW and BW are closely linked and positioned near to an elevation of 125 m, indicating a higher frequency at this elevation, and microhabitat UR shows a distinct association with elevation compared to DW and BW. Elevations 325 and 488 m closely align with microhabitat DT.
An analysis of the distribution of termite species across four microhabitats reveals a significant association (χ2 = 122.08, df = 6, p < 2.2 × 10−16), indicating distinct habitat preferences among the studied species (Figure 7).
The mean density of termites in the cork oak forest, situated at lower elevations, is notably higher at 0.06 ± 0.008 hits/m2 compared to the holm oak forest (0.04 ± 0.014 hits/m2) and the fir and cedar forests at 0.02 hits/m2 (±0.009 and ± 0.006, respectively) (Supplementary Material, Table S3).
The analysis of variance (ANOVA) conducted to investigate the effect of forest type on termite density revealed a non-significant trend (F = 2.378, df = 3, p = 0.075). The boxplot showed that the QS forest has the highest and most variable termite density, while the CA forest has the lowest. QI and AM forests showed similar densities (Figure 8).

4. Discussion

Studies on biodiversity along elevation gradients have been reported for many taxa worldwide [30]. The responses of different groups of arthropods, including spiders, millipedes, centipedes, ants, ground beetles, and rove beetles, to elevation variations have been investigated in the Swiss Alps. The study revealed diverse trends depending on the taxa examined, but elevation was more important than most local soil and vegetation characteristics [31].
Within the confines of our main study area, only beetles, dipterans, and ants have been subject to investigation, while other taxonomic groups have not yet received dedicated attention. Previous research efforts [32,33,34,35,36,37,38] have predominantly concentrated on these three groups. Notably, termites have not undergone ecological exploration, either within our study area or, more broadly, in Morocco.
At the elevational gradient studied in the western Rif Mountains of northern Morocco, R. grassei was the most abundant species, accounting for over half of the observations, followed by K. flavicollis and Amitermes sp. It is a subterranean termite native to the Iberian Peninsula and France [15]. Its geographical distribution has expanded globally in recent years. It has been reported in Devon (United Kingdom) and Horta (Faial Island, Azores) [39,40], as well as in the canton of Zurich in Switzerland [41], on Madeira and Azores Islands [14]. Regarding its presence in Morocco, this species is a relatively recent discovery. The first reports were in Ifrane and Ajabo, Meknes province, Assilah, Tanger province [15], and in the Bouhachem Natural Park, Tetouan province [14]. Therefore, our observation represents the third citation of the species in Morocco and the first record for TLSNP. However, the phylogenetic relationships of Moroccan populations with European Reticulitermes termites remain unclear, with a potential presence of more than one species [15]. The drywood termite K. flavicollis, which has a Mediterranean distribution, is found in Southern Europe (Spain, Portugal, France, Italy, Croatia, Greece and Slovenia), the Near East (Israel, Syria, and Tukey) and North Africa (Morocco, Algeria, Libya, Tunisia and Egypt) [11,39]. It was first reported in Morocco during its description by Sjöstedt in 1904 under the name Calotermes maroccoensis. This species was collected by Buchet in 1901 in Tangier, as indicated on the label of the paratype specimen deposited in the Paris Museum (syntype) [42]. The species was reported recently in Meknes by David Mora in 2018 [43]. Thus, our capture represents the third record of K. flavicollis in Morocco and the first for the TLSNP. The only recorded observation of the genus Amitermes in Morocco dates back to 2017 in Machraà Ben Abbou, Settat province, in a semi-arid climate, without the species being identified [43]. Our discovery of specimens from the same genus in a completely different subhumid habitat prompts us to undertake a comprehensive taxonomic revision of this genus in Morocco. In North Africa, only two Amitermes species have been documented during their descriptions: A. messinae Fuller 1922 in Egypt (Fuller, 1922) and A. desertorum (Desneux, 1902) in Algeria, Tunisia, Libya, and Egypt (Desneux, 1902). These two species are subterranean termites perfectly adapted to arid and desert environments [29,44]. However, it is worth mentioning that the single observation of the genus Amitermes in Morocco does not mention any species [43].
Regarding species richness, our results agree with those obtained in the Leuser ecosystem, where the pattern of decreasing diversity with an increasing elevation gradient was monotonous [23]. At higher elevations, temperatures tend to be lower, which can constrain termite activity, while food resources may become scarcer. The decline in termite species composition with increasing elevation is attributable to the reduction in temperature, which affects their metabolic rates [23]. This hypothesis is supported by the fact that air temperatures decrease by an average of 1 °C for every 100 m increase in elevation. Other factors could contribute to a monotonic decline in termite species composition along the elevation gradient, including variations in food availability, soil structure, or other habitat characteristics associated with changes in elevation [16,45]. Our study revealed a moderate negative correlation between elevation and the density of termite nests. This finding implies that the sensitivity of termites to environmental changes associated with elevation and resource availability could influence not only species richness but also termite density. Furthermore, the elevation gradient has a significant effect on the density and abundance of termites on the Amazon–Andes, where the number of soil feeders declined between 925 and 1500 m, while wood feeders declined between 1550 and 1850 m [22]. Additional instances of mid-elevation peaks in termite diversity. However, these peaks were attributed to disturbances from human activities and the limited elevation range of their study areas [46,47]. Nevertheless, these explanations do not apply to our study since most of our sampling sites are located within a protected area.
As for their microhabitats, in Mediterranean forests, termites occupy microhabitats that exhibit significant differences compared to those found in tropical forests [48]. There is a greater diversity of microhabitat categories at lower elevations, with an increased availability of deadwood, which is less common at higher elevations [22]. This suggestion is accurate with our study, in which the association of the DW, BW, and DT categories with elevation indicates more microhabitats for termite presence at lower elevations. This aligns with the case observed for K. flavicollis (dry wood feeders), predominantly located in DT and DW microhabitats at lower elevations but also at a much higher altitude probably related to the presence of a suitable microhabitat (DT). In contrast, R. grassei and Amitermes sp. (wood feeders in the soil) were detected in BW and UR microhabitats. Amitermes sp., despite having a microhabitat available, was only detected at low elevations. R. grassei exhibited a more even distribution in these microhabitats along the gradient, indicating their adaptability to different environmental conditions, as occurs in the Iberian Peninsula ranging from sea level to high elevations.
As ectothermic fauna, the body temperature of termites depends on environmental temperature, but responses vary depending on termite species [22,23,24,25,26,27,28,29,30,31,32,33,34,35,36,37,38,39,40,41,42,43,44,45,46,47,48,49]. Wood has a very high carbon: nitrogen ratio (C: N) and therefore, N is usually limited. More humified material as decayed substrates has a higher nitrogen content [50]. It has been assumed that Reticulitermes obtains micronutrients and nitrogen from the soil in the form of nitrate to balance the low nitrogen content of wood [51]. This may be the reason why it can live at higher elevations despite lower temperatures. In the case of Amitermes sp., as they are associated with desertic or dry habitats, they may be excluded from the more humid upland areas of the study [44]. Kalotermitidae fixes nitrogen from the atmosphere via symbiotic gut bacteria [50]. Kalotermes flavicollis can probably live at more than 1000 m and obtain nitrogen using this method as long as there is dry wood. In addition, the four elevations at which this species was found are dominated by Quercus suber forest formations.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/d16120714/s1, Table S1. Mean density of all termite species per m2 in each site along an elevational gradient in Northwestern African mountains; Table S2. Contingency table of termite microhabitats by elevation. Abbreviations: BW: buried dead wood; DT: dead trunk; DW: dry dead wood; and UR: under rock. Table S3. The mean density of the three captured termite species across the forest types (hits/m2).

Author Contributions

Conceptualization, A.N., D.H.-T. and A.T.; Methodology, D.H.-T.; Validation, D.H.-T. and A.T.; Formal Analysis, A.N. and A.T.; Investigation, A.N., B.E.A. and A.T.; Data Curation, A.N. and A.T.; Supervision, A.T. and D.H.-T.; Writing—Original Draft Preparation, A.N. and A.T.; Writing—Review and Editing, D.H.-T., B.E.A., Y.B. and A.T. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding. David Hernández-Teixidor was funded by the Cabildo de Tenerife.

Institutional Review Board Statement

Not applicable.

Data Availability Statement

The original contributions presented in this study are included in the article/Supplementary Material.

Acknowledgments

We thank the “National Agency for Water and Forests” of the Kingdom of Morocco for providing us with the scientific permit to collect the samples cited in this article (Decision N°16/2022). We thank James Wetterer (Florida Atlantic University, USA) for his help with the English language, and Ikssi Mohamed and Abderrahmane El Boukhrissi (University of Abdelmalek Essaâdi-Tetouan, Morocco) for their help in creating the elevational map.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Elevational map of the study area with the location of the nine sampling stations (Northwest Morocco, Northwest Africa). Abbreviations: TLSNP; the Talassemtane National Park. IMBR; Intercontinental Mediterranean Biosphere Reserve; S1–S9; sampling stations.
Figure 1. Elevational map of the study area with the location of the nine sampling stations (Northwest Morocco, Northwest Africa). Abbreviations: TLSNP; the Talassemtane National Park. IMBR; Intercontinental Mediterranean Biosphere Reserve; S1–S9; sampling stations.
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Figure 2. The four categories of termite microhabitats in the study area. (A) Microhabitat of surface soil (under rocks); (B) dry dead wood (trunks and branches on the ground surface); (C) dead trunk fixed to the ground (dry wood in the superior part); (D) buried dead wood (damp wood with galleries in the ground).
Figure 2. The four categories of termite microhabitats in the study area. (A) Microhabitat of surface soil (under rocks); (B) dry dead wood (trunks and branches on the ground surface); (C) dead trunk fixed to the ground (dry wood in the superior part); (D) buried dead wood (damp wood with galleries in the ground).
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Figure 3. Dorsal view of termite species (soldier). (a) Kalotermes flavicollis; (b) Reticulitermes grassei; (c) Amitermes sp.
Figure 3. Dorsal view of termite species (soldier). (a) Kalotermes flavicollis; (b) Reticulitermes grassei; (c) Amitermes sp.
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Figure 4. The variation in termite density (hits/m2) along the elevation gradient. (A) Mean termite density with regression trend (blue line) and confidence interval (grey band); (B) density of Kalotermes flavicollis (rs = −0.5145; p = 2.1365 × 10−7); (C) density of Amitermes sp. (rs = −0.3963; p = 0.0001); (D) density of Reticulitermes grassei (rs = −0.0057; p = 0.9575).
Figure 4. The variation in termite density (hits/m2) along the elevation gradient. (A) Mean termite density with regression trend (blue line) and confidence interval (grey band); (B) density of Kalotermes flavicollis (rs = −0.5145; p = 2.1365 × 10−7); (C) density of Amitermes sp. (rs = −0.3963; p = 0.0001); (D) density of Reticulitermes grassei (rs = −0.0057; p = 0.9575).
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Figure 5. Distribution of microhabitats per elevation. Abbreviations: BW: buried dead wood; DT: dead trunk; DW: dry dead wood; and UR: under rock.
Figure 5. Distribution of microhabitats per elevation. Abbreviations: BW: buried dead wood; DT: dead trunk; DW: dry dead wood; and UR: under rock.
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Figure 6. Correspondence analysis factor map of microhabitats (red triangle) by elevation level (blue point). Numbers correspond with the elevations of each station. Abbreviations: BW: buried dead wood; DT: dead trunk; DW: dry dead wood; and UR: under rock.
Figure 6. Correspondence analysis factor map of microhabitats (red triangle) by elevation level (blue point). Numbers correspond with the elevations of each station. Abbreviations: BW: buried dead wood; DT: dead trunk; DW: dry dead wood; and UR: under rock.
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Figure 7. Distribution of termite species across microhabitats. Abbreviations: BW: buried dead wood; DT: dead trunk; DW: dry dead wood; and UR: under rock.
Figure 7. Distribution of termite species across microhabitats. Abbreviations: BW: buried dead wood; DT: dead trunk; DW: dry dead wood; and UR: under rock.
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Figure 8. Boxplot analysis of termite density variability by forest type. Abbreviations: QS: Quercus suber; QI: Quercus ilex; AM: Abies marocana; CA: Cedrus atlantica.
Figure 8. Boxplot analysis of termite density variability by forest type. Abbreviations: QS: Quercus suber; QI: Quercus ilex; AM: Abies marocana; CA: Cedrus atlantica.
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Table 1. Elevation distribution and habitat characteristics of studied sites in Northwestern African mountains.
Table 1. Elevation distribution and habitat characteristics of studied sites in Northwestern African mountains.
CodeSitesElevation (m)LatitudeLongitudeDominant Tree SpeciesProtected Area
Site 1Hjar Nhal, Tanger12535.588−5.915Quercus suberNo
Site 2Jbel hbib, Tetouan32535.436−5.767Quercus suberNo
Site 3Derdara, Chefchaouen48835.099−5.302Quercus suberNo
Site 4Bghaghza 1, Tetouan71535.434−5.636Quercus suberNo
Site 5Bghaghza 2, Tetouan85035.420−5.623Quercus suberNo
Site 6TLSNP, Chefchaouen115035.074−5.173Quercus suberYes
Site 7TLSNP, Chefchaouen131635.097−5.145Quercus ilexYes
Site 8TLSNP, Chefchaouen154435.115−5.134Abies marocanaYes
Site 9TLSNP, Chefchaouen170035.140−5.137Cedrus atlanticaYes
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Najjari, A.; Hernández-Teixidor, D.; El Ajjouri, B.; Benyahia, Y.; Taheri, A. Termite (Blattodea: Isoptera) Distribution Along an Elevational Gradient in Northwestern African Mountains. Diversity 2024, 16, 714. https://doi.org/10.3390/d16120714

AMA Style

Najjari A, Hernández-Teixidor D, El Ajjouri B, Benyahia Y, Taheri A. Termite (Blattodea: Isoptera) Distribution Along an Elevational Gradient in Northwestern African Mountains. Diversity. 2024; 16(12):714. https://doi.org/10.3390/d16120714

Chicago/Turabian Style

Najjari, Aya, David Hernández-Teixidor, Bilal El Ajjouri, Yousra Benyahia, and Ahmed Taheri. 2024. "Termite (Blattodea: Isoptera) Distribution Along an Elevational Gradient in Northwestern African Mountains" Diversity 16, no. 12: 714. https://doi.org/10.3390/d16120714

APA Style

Najjari, A., Hernández-Teixidor, D., El Ajjouri, B., Benyahia, Y., & Taheri, A. (2024). Termite (Blattodea: Isoptera) Distribution Along an Elevational Gradient in Northwestern African Mountains. Diversity, 16(12), 714. https://doi.org/10.3390/d16120714

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