Research Article |
Corresponding author: Soumia Moutaouakil ( moutaouakil.soumia@gmail.com ) Corresponding author: Marconi Souza-Silva ( marconisilva@dbi.ufla.br ) Academic editor: Ľubomír Kováč
© 2024 Soumia Moutaouakil, Marconi Souza-Silva, Lais Furtado Oliveira, Mohamed Ghamizi, Rodrigo Lopes Ferreira.
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:
Moutaouakil S, Souza-Silva M, Oliveira LF, Ghamizi M, Ferreira RL (2024) A cave with remarkably high subterranean diversity in Africa and its significance for biodiversity conservation. Subterranean Biology 50: 1-28. https://doi.org/10.3897/subtbiol.50.113919
|
Aziza cave, which is also known as kef Aziza or Tazouguert cave, represents an important and large karstic system that consists of more than 3.5 km of surveyed galleries, standing as the fifth most extensive cave system in Morocco and one of the ten largest in North Africa. This study unveils Aziza cave as an important spot of subterranean diversity in Africa. Here, we provide the first checklist of subterranean fauna in this cave, with 26 taxa, comprising 22 troglobiotic and 4 stygobiotic species. Of this total, eight species still require further confirmation of their status. The richest taxa include Coleoptera (5 species), Araneae (4 species), Entomobryomorpha (3 species), and Isopoda (2 species). However, it is noteworthy that only around 34.6% of the cave-restricted species found in the cave have been formally described to date. Additionally, the biodiversity of large system areas remains to be discovered as these areas need to be further explored. Furthermore, this paper highlights the broader conservation challenges faced by subterranean habitats in Morocco, particularly considering human-induced impacts on these remarkable ecosystems. We aim to draw attention to the crucial ecological role of subterranean environments and their extraordinary biological diversity. By doing so, we aim to inspire increased research and conservation initiatives, not just in this area but across Africa.
Aziza, cave conservation, cave diversity, Noth-Africa, protection strategies
Subterranean ecosystems play a significant role, serving as crucial freshwater reservoirs on a global scale (
Several regions worldwide are renowned for hosting hotspots of subterranean biodiversity (HSB), as evidenced in various studies (
Among the most well-known is the Dinaric Karst in Balkan Peninsula, extending through several Balkan countries, which provides a habitat for a rich diversity of cave-dwelling species (
However, given the arbitrary cutoff number for defining HSB, it is crucial to identify sites or caves with a remarkable diversity of cave-restricted species, even if their count does not reach the minimal cutoffs. This is important for two reasons: (i) the concept of “high diversity” is often context-dependent, varying with the area where a cave is located, and (ii) new species can be discovered even in well-studied caves, as the subterranean realm extends beyond the accessible macrocaverns. Therefore, identifying and emphasizing caves with a high diversity of cave-restricted fauna holds significant potential for conservation efforts and the establishment of specific protection policies. The specialized adaptations and limited distributions of several subterranean species render them highly susceptible to habitat loss and degradation. As such, the identification and conservation of these hotspots play a pivotal role in ensuring the long-term survival of this exceptional, significant, and fascinating fauna (
Some areas in Africa have been studied by speleologists (Juberthie and Decu 1994), and a short survey of highly biodiverse cave regions in Africa can be found in
This paper highlights the occurrence of a cave with a remarkable subterranean diversity in Africa, known as the Aziza cave (also referred to as Tazouguert cave and locally as Kef Aziza), located in Morocco. Our study analyzes the cave’s distinctive geological and hydrological characteristics and the diverse species inhabiting this unique ecosystem. Additionally, we address the conservation challenges that some subterranean habitats in Morocco face, particularly concerning human-induced impacts on subterranean species. By highlighting these ecosystems and their exceptional biodiversity, we aim to inspire more research and conservation efforts in this region and across Africa.
The Aziza cave is located in the Tazzouguert Plateau, within the administrative boundaries of the Oued Naam commune near Boudnib town, in the province of Er-Rachidia, within the Drâa Tafilalt region of eastern Morocco (Fig.
The Aziza cave is situated in a pre-Saharan zone of Morocco (
The area is part of the Guir’s Hamada, a plateau spanning approximately 1000 square kilometers. This plateau is primarily composed of sedimentary layers of Cenomanian-Turonian limestone, consisting of bioclastic limestones with bryozoans and stromatoporidae, followed by marl limestones containing bioclastic ammonites, lamellibranches, echinoderms, gastropods, and bryozoans (Ettachfini et al. 2020).
The Cretaceous sedimentary basin in the region comprises three overlapping exploitable aquifers. Below is an impermeable substratum of Cenomanian Marl (Infracenom), while Senonian sandstones and clay sands are above. Between these layers exists the Turonian, which serves as the primary aquifer in the basin. The thickness of this reservoir varies between 20 and 100 meters. Fissures and karstification of the limestone formations contribute to the formation of several springs, such as Mouy (Qm p 80 l/s), Tamazirt (Qm p 135 l/s), Meski (Qm p 167 l/s), and others, along with the underground network of the Aziza cave, which is classified as hypogenic (El Ouali et al. 1999; Audra 2017).
The province’s economy relies heavily on agriculture, making it highly dependent on water resources. Moreover, the region faces several challenges, including soil and water salinization, desertification, and silting. These challenges exacerbate the region’s vulnerability, underscoring the urgent need for sustainable strategies to mitigate their impacts (
Aziza Cave (32.0146°N, -3.4717°W) is situated in the Eastern High Atlas, approximately 80 kilometers from Errachidia city towards Boudnib, at an elevation of 1059 m above sea level (
The gallery of the cave gently descends, featuring some meanders and detours while maintaining a consistent SE-NW orientation. The first part of the cave features remarkable and expansive dimensions. After about 450 m from the entrance, one reaches the Guano Room (large cavities in Fig.
The location of Aziza Cave near the Guir River suggests that it might have served as an insurgence of the river during periods when the water level was higher than the current cave entrance. However, a study conducted by a Croatian team in 2003 proposed an alternative hypothesis, suggesting that the cave’s formation occurred in two distinct stages. The first stage involved a phreatic genesis underground, which was ancient and led to fossilization. During this phase, the slope of the cave might have been lowered due to the erosion caused by the Oued Guir, possibly affecting a part of the cave system. Subsequently, a second phase occurred, which is more recent and primarily affected the deeper parts of the cave through vadose processes. This second phase is not directly linked to the genesis of the main cave system. Instead, it is believed to have evolved in drier climates with well-developed speleogenetic mechanisms, possibly influenced by different lithotypes and favored by widespread absorption on heavily cracked plains of the hamada (
The presence of bats has also significantly influenced the cave’s morphology. Biogenic corrosion, caused by the secretions of these animals, has had a profound impact on the condition of the cave walls and roofs. The mineralized urine droplets directly attack the surrounding limestone, leading to corrosion over time. Moreover, the combination of ammonia from urine and CO2 from bats’ respiration produces carbonic acid through condensation, further extending the corrosion process. As a result of these physicochemical processes, the main gallery now exhibits various unique features, including ceilings with bell holes, hemispherical domes, and smooth walls, which have erased the original morphologies of the cave (Fig.
The first known explorations of Aziza Cave date back to 1925, followed by another expedition in 1948 (
1970 a Spanish expedition explored only 1000 meters of the cave (
Aziza cave has been the subject of several biospeological expeditions over the years. The first survey was conducted in 1968 by the Atlas Expedition of “Equip de Recerques Espeleològiques from the Centre Excursionista de Catalunya” (Canals and Viñas 1969;
The data on the Aziza cave fauna was gathered by conducting a comprehensive literature search, focusing on relevant keywords such as “African cave biodiversity,” “Aziza,” “Tazouguert,” “cave fauna,” “troglobitic fauna,” “stygobitic fauna,” “groundwater,” “pollution,” and “North Africa.” We selected the most pertinent databases that contained information related to cave biodiversity.
To investigate the spatial variation of temperature and humidity within the cave, we used temperature and humidity data loggers (accuracy ± 1 °C for temperature and ± 5% for relative humidity). Starting from the cave entrance, we positioned the instrument on the cave floor and recorded data for 15 minutes (
to create a comprehensive documentation of invertebrate species to the cave environment, we used various search methods to thoroughly investigate the different microhabitats within the cave (
The terms stygobionts and troglobionts encompass species that live in caves and various shallow subterranean and above-ground habitats. While most subterranean species typically display troglomorphy, including reduced eyes and pigment, increased size, elongated appendages, and extra-optic sensory structures, certain troglobionts may exhibit limited or no troglomorphy due to factors such as habitat volume, twilight exposure, isolation age, genetic variability, and others. This variability suggests some species may qualify as eutroglophiles (
Species restricted to subterranean environments, such as troglobionts and stygobionts, cannot complete their life cycles in aboveground habitats (
While troglomorphisms offer valuable insights into the potential status of species, their analysis must consider the contexts of the external ecosystems surrounding caves (
Based on our recent cave explorations and a review of existing literature, we have assessed and categorized human interactions with modifications to the cave and its surrounding areas. Our evaluation, guided by the framework established by
The cave displayed distinct conditions within its inner regions. Close to the entrance, the air was noticeably dry (up to 80 m – 62.4% moisture content), while deeper inside (after 100–150 m), it became increasingly humid (reaching 98.2% moisture content after 800–850 m), resulting in a diverse and heterogeneous cave ecosystem concerning humidity levels. The average air temperature inside the cave hovered around 23 °C (±1.5), with inner portions maintaining an average air moisture of about 80% (±18). The cave floor displays organic and inorganic materials such as bat feces, plant debris (from torches used by visitors), and various types of clastic sediments, ranging from large rocks to gravel, sand, silt, mud, and hardpan. This diverse mix of materials allows for different microhabitats with varying characteristics as you move from the cave entrance to its deeper sections. Notably, the substrate composition near the entrance showed more diversity, while it became less varied in the deeper parts of the cave.
The primary sources of nutrients for terrestrial and aquatic fauna within the cave are guano and bat carcasses. Additionally, plant debris is scattered throughout the cave, displaying various degrees of decomposition (Fig.
In May 2002, the cave hosted several colonies of Rhinolophus euryale Blasius, 1853, and Myotis punicus Felten, Spitzenberger & Storch, 1977. These bats were mostly found scattered across the ceiling of the large chamber, approximately 450 meters from the cave’s entrance (Fig.
The discovery of some bat corpses enabled species identification through bone measurements, revealing the presence of a fourth species: Miniopterus schreibersii (Kuhl, 1817). In 2014, the Aziza cave was designated as the type locality for a new species: Miniopterus maghrebensis Puechmaille, Allegrini, Benda, Bilgin, Ibañez & Juste, 2014 (Puechmaille et al. 2014). This discovery increased the diversity of bats in this cave, bringing the total number to five species.
To date, 26 troglobitic and stygobitic species have been documented within Aziza cave, comprising 22 troglobiotic and 4 stygobiotic species. Of this total, eight species still require further confirmation of their status; thus, at least 18 are cave-restricted. These species are distributed across several taxonomic groups: Arachnida (7 species), Insecta (6 species), Crustacea (4 species), Collembola (4 species), Chilopoda (2 species), Gastropoda (2 species), and Diplopoda (1 species) (Table
Some of the species restricted to the Aziza cave, Morocco. Castellanethes sp. 1 (A), Magnezia gardei (B), Arrhopalites sp. 3 (C), Scaurus tingitanus gimeli (D), Apteranillus ruei (E), Tychobythinus sp. (F), Dysdera sp. 1 (G), Dysdera caeca (H), Lepthyphantes fadriquei (I), Parasitengona sp. 1 (J), Eukoenenia maroccana (K), Geophilomorpha sp. 1 (L), Jeekelosoma abadi (M), Cryptops (Trigonocryptops) aff. numidicus aelleni (N), Eupumonata sp. 24 (O).
In Aziza Cave, terrestrial invertebrates rely on plant debris (A, B, C) and small guano pellets (D) as sources of nutrients. Specimens of J. abadi forage on plant debris for sustenance, indicated by red circles in section C. Additionally, the red arrow in section D highlights the presence of J. abadi specimens foraging on guano pellets.
The Aziza cave in Er-Rachidia, Morocco, is home to a diverse array of terrestrial and aquatic obligate cave-dwelling invertebrates. Unidentified (un). TB -Troglobite; SB - Stygobite; TB? - Potential troglobionts (further studies needed for confirmation).
Taxon | Taxon | Family name | Species/morphotypes | Status |
---|---|---|---|---|
Arachnida | Acari | Parasitengona | Parasitengona sp. 1 | TB? |
Araneae | Hahniidae | Hahniidae | TB | |
Dysderidae | Dysdera sp. | TB | ||
Dysdera caeca Ribera, 1993 | TB | |||
Linyphiidae | Lepthyphantes fadriquei Barrientos, 2020 | TB | ||
Palpigradi | Eukoeneniidae | Eukoenenia maroccana Barranco an Mayoral, 2007 | TB | |
Pseudoscorpiones | Chthoniidae | Chthoniidae sp. | TB? | |
Collembola | Symphypleona | Arrhopalitidae | Arrhopalites sp. | TB? |
Entomobryomorpha | un | Entomobryidae sp. 1 | TB? | |
un | Entomobryidae sp. 2 | TB? | ||
un | Isotomidae sp. 1 | TB? | ||
Insecta | Coleoptera | Carabidae | Platyderus insignitus presaharensis Lagar Mascaró, 1978 | TB |
Curculionidae | Torneuma troglodytis Stüben, 2009 | TB | ||
Pselaphinae | Tychobythinus sp. | TB? | ||
Staphylinidae | Apteranillus ruei Español, 1969 | TB | ||
Tenebrionidae | Scaurus tingitanus gimeli Peyerimhoff, 1948 | TB | ||
Sternorrhyncha | Kinnaridae | Kinnaridae sp. | TB | |
Diplopoda | Polydesmida | Paradoxosomatidae | Jeekelosoma abadi Mauriès, 1985 | TB |
Chilopoda | Scolopendromorpha | Cryptopidae | Cryptops (T.) aff. numidicus aelleni Manfredi, 1956 | TB? |
Geophilomorpha | un | Geophilomorpha sp. | TB? | |
Crustacea | Bathynellacea | Bathynellaceae | Bathynellaceae sp. | SB |
Isopoda | Ollibrinidae | Castellanethes sp. | TB | |
Asellota | Stenasellidae | Magnezia gardei Magniez, 1978 | SB | |
Copepoda | un | Copepoda sp. | SB | |
Gastropoda | Eupumonata | un | Eupulmonata sp. | TB? |
Neotaenioglossa | Hydrobiidae | Hydrobiidae sp. | SB |
Notably, only around one-third (34.6%) of the cave-restricted species found in the cave have been formally described to date. These described species include Dysdera caeca Ribera, 1993, Lepthyphantes fadriquei Barrientos, 2020, Eukoenenia maroccana Barranco & Mayoral, 2007, Platyderus insignitus presaharensis Lagar Mascaró, 1978, Torneuma troglodytis Stüben, 2009, Apteranillus ruei Español, 1969 (
Regarding the aquatic fauna, Aziza Cave has revealed the presence of four stygobiont species: the isopod Magniezia gardei, a hydrobiid gastropod, a copepod species, and a Bathynellacea species. The first two species are found in a small, clayey substrate puddle 4 meters in length and 1 meter in depth, located in the left branch 1000 meters from the entrance (Figs
Magniezia gardei was first described from Aziza Cave but has a relatively broad distribution, having been found in several wells in the Errachidia and Zagora regions (
The terrestrial fauna in Aziza Cave exhibits remarkable diversity, comprising 22 troglobitic and/or troglomorphic species (Table
Regarding their sampling areas, Hahniidae sp. were observed 400 meters from the entrance, while the Coleoptera Scaurus tingitanus gimeli is distributed between 200 meters and 800 meters. Because the species is only known from caves and appears absent on the surface (assuming adequate sampling in the area), it is justifiable to categorize it as a troglobiont, regardless of the
A solitary individual of Chthoniidae sp. was captured 600 meters from the entrance, near the remains of a mammal (sheep or goat bones were observed).
Several species are endemic to this cave, including the Diplopoda Jeekelosoma abadi, the Araneae Dysdera caeca and Lepthyphantes fadriquei, and the Palpigradi Eukoenenia maroccana. These species are distributed in the explored part of the cave beyond the guano room, a large cavity depicted in Fig.
The coleopteran Pselaphinae Tychobythinus sp., the Sternorrhyncha Kinnaridae sp., and the Geophilomorpha sp. were collected in clayey habitats with humidity levels close to saturation (over 98%) after 800 meters from the entrance. The species of Kinnaridae was collected near the third siphon.
In addition to its proximity to a town (Boudnib, 19.7 km), the cave is situated near a paved road (Fig.
Human activities have significantly impacted the Aziza caves and their surrounding area. The construction of roads and using tractors near the riverbed have affected the caves directly, particularly entrances (A, B). Additionally, the caves have been marred by the deposition of garbage at entrance C and graffiti along the cave walls at positions D, E, F, G.
The initial section of the cave, easily accessible to visitors, has unfortunately been heavily impacted by graffiti and trampling. As one approaches the entrance, litter and shattered rocks, along with fragments of glass and plastic, can be observed (Fig.
The Aziza Cave stands out as a significant subterranean habitat, presenting 18 troglobiotic and stygobiotic species, plus eight taxa that may also represent cave-restricted species, making it the richest cave regarding troglofauna and stygofauna in Africa. The second richest cave is the Wynberg Cave System, located in the mountains of Cape Town, South Africa, which hosts 19 cave-restricted species (Ferreira et al. 2021). It is worth mentioning that although the Wynberg Cave System has not been officially proposed as a subterranean biodiversity hotspot, it indeed represents a hotspot in the African continent, based on criteria proposed by
The high number of cave-restricted species in Aziza Cave can be attributed to a combination of factors. Firstly, its location in the Sahara Desert gives this cave a unique setting, distinguishing it from the arid and harsh surface environment. The high and constant humidity conditions within the cave starkly contrast with the arid surroundings. The species richness may also be linked to historical climatic changes in the region where the cave is situated (
Furthermore, the substantial size of the cave, stretching approximately 4 kilometers, provides ample space for the development of several microhabitats, which can support various distinct invertebrate taxa. Lastly, the presence of subterranean water bodies further enhances the diversity of terrestrial and aquatic habitats available for colonization by the fauna. It is important to mention that a high richness of cave-restricted species is often associated with large subterranean spaces, high productivity, and/or isolated water bodies separate from the surface (Culver and Pipan 2009). These factors collectively contribute to the remarkable biodiversity observed in Aziza Cave.
The distribution and degree of adaptation of most cave-dwelling invertebrates within caves are often more influenced by the physical environment of the cave rather than by food resources or cave geology (Novack et al. 2012;
The apparent scarcity of Subterranean Biodiversity Hotspots in Africa is a noteworthy issue. Despite the continent’s vast expanse and its potential for hosting unique subterranean ecosystems, there has been limited exploration and documentation of these habitats. This dearth of attention to subterranean biodiversity has led to significant knowledge gaps, impeding our understanding of the richness and ecological importance of these ecosystems in most parts of the continent.
While the biodiversity of Aziza Cave has been extensively documented, it is important to highlight that the current fauna list is likely incomplete. There are still unexplored areas within the cave that necessitate comprehensive biological inventories. Furthermore, many microhabitats have not been adequately sampled, as specific techniques for sampling smaller invertebrates in terrestrial and aquatic habitats were not employed, as mentioned in the methodology.
We must not assume that the species richness of a subterranean habitat is fully known, which is why new explorations are often necessary (
On the other hand, according to
Conserving the fauna of Aziza Cave presents a significant challenge, as it is impacted not only by local factors but also by local and global climate issues (
Aziza Cave is situated within the UNESCO Biosphere Reserve, Oasis du Tafilalet (Ramsar site no. 1483), a site of significant biological and ecological importance. Oasis du Tafilalet is in Errachidia, Goulmima, Sahara SE Morocco (31°17'N, 004°15'W), covering an area of approximately 1,370 km2. The site encompasses a series of oases, serving as the reservoir for one of Morocco’s oldest dams, Hassan Ad-Dakhil, which contains small rivers, irrigation channels, and lagoon areas. It serves as an essential wintering ground for migratory birds and is home to notable populations of Rüppell’s pipistrelle bat (Pipistrellus rueppelli). Agriculture is a prominent activity in the region, with Alfalfa, cereals, henna, date palms, and fruit trees being the primary crops. Sheep farming is also prevalent.
However, the management of dam water releases downstream has resulted in some channels having water only during specific times of the year, further exacerbated by excessive water abstraction for agriculture and human consumption, along with the increased frequency of droughts in recent decades. Additionally, soil salinization has become a problem in various areas due to high evaporation rates (
Subterranean habitats, such as caves, are relatively unexplored environments with limited attention due to their challenging accessibility (
When
In this context, relying solely on the richness of troglobiotic species may not accurately reflect the “health” of a specific subterranean system, as this will depend on the type of impact it has endured (
Numerous conservation efforts have been undertaken worldwide to safeguard subterranean habitats, their fauna, and the ecosystem services they provide. A comprehensive global assessment, drawing from the opinions of over 150 experts, has identified that legislation, public policies, landscape protection and management, and environmental education constitute the most crucial conservation measures (
Conservation based on establishing legally protected areas and their proper management has been widely recognized as one of the most effective strategies to combat biodiversity loss in various ecosystems (
Promoting awareness campaigns, adopting responsible practices, and embracing sustainable approaches must be the focal point of our conservation endeavors, particularly in the case of Aziza Cave, which harbors such diversity of cave-dwelling invertebrates. Cultivating deep respect for these fragile environments among the local population and implementing effective conservation strategies are paramount. Through these endeavors, we can ensure the enduring survival and safeguarding of these subterranean treasures for the benefit of future generations (
Finally, addressing these challenges requires concerted efforts to increase sampling and exploration activities in African caves and other subterranean environments. By focusing on areas with high potential for cave-restricted species, researchers can contribute to identifying and designating new Subterranean Biodiversity Hotspots on the continent. These designated hotspots will serve as focal points for conservation and research initiatives, allowing us to protect better and comprehend the unique life forms that thrive in these underground realms.
Laís Furtado Oliveira was sponsored by Capes Foundation (Coordination for the Improvement of Higher Education Personnel) with 48 months of scholarships. Rodrigo Lopes Ferreira thanks the National Council for Technological Development and Scientific Development (CNPq) for research grant nº 302925/2022-8. We are thankful to Guilherme Prado (Pseudoscorpiones), Giovanna Monticelli Cardoso (Isopods), Leopoldo Bernardi (Acari), and Sylvain Lecigne (Araneae) for their help in identifying the fauna. We thank VALE/SA for financial support. A special thanks to Abderrahim S’khifa and Jean-Philippe Degletagne for their assistance in the fieldwork