Imarhiagbe and Aighokan Proceedings of 7th NSCB Biodiversity Conference, October 2020 Evaluation of the Conservation Status of Thonningia sanguinea Vahl. (Balanophoraceae) and Threats to its Survival in Southern Nigeria *1 IMARHIAGBE Odoligie and 2AIGBOKHAN Emmanuel Izaka Department of Biological Science, Edo University Iyamho, Edo State, Nigeria 2 Department of Plant Biology and Biotechnology, University of Benin, Benin City, Nigeria *Corresponding e-mail: imarhiagbe.odoligie@edouniversity.edu.ng; Phone: +2348031984621 1 ABSTRACT Thonningia sanguinea Vahl. Balanophoraceae, a cryptic parasitic plant, is among the poorly understood, yet understudied afro-tropical endemic taxa. This study assessed the conservation status and identified possible threats to the survival of T. sanguinea in southern Nigeria. Data on the distribution, population and possible threats were collected from field survey in twenty-one (21) selected locations. Additionally, 104 residents were interviewed in the study areas. Overall, forty-nine (49) T. sanguinea populations were identified across the selected locations. The results showed that host tree species such as Guarea cedreta (Meliaceae), Hevea brasiliensis (Euphorbiaceae), Lophira alata ((Ochanaceae) Musanga cecropiodes (Urticaceae), Myrianthus arboreus (Urticaceae), Ricinodendron heudelotii (Euphorbiaceae), Theobroma cacao (Malvaceae) supported the T. sanguinea populations in the area. However, threats to T. sanguinea populations were habitat loss and degradation, bushfire, and destructive feeding by some forest ruminants. Although, from the IUCN Red list analysis, the status of T. sanguinea is Near-threatened (NT), findings from this study suggests that in the near future it could qualify for a threatened category from continued threat to the survival. It is recommended, therefore, that the identified T. sanguinea populations from this study should be protected and allowed to proliferate with the host plant species. Keywords: Thonningia sanguinea, Conservation, Near Threatened, Southern Nigeria. However, due to the possibility of local extinction of INTRODUCTION Conservation of rare and endangered species species occurring at different scales in different regardless of their troublesomeness or usefulness to locations, there became a need for a well-suited humans should be of utmost priority. Among the guideline for assessment on a national scale. For components of biodiversity to be protected, attention instance, a species with a wide distribution may well is scarcely being given to the conservation of have a low risk of becoming extinct globally (and parasitic species. This is so because most parasitic hence it may be listed as Least Concern on The plants are often viewed as pests, causing destructive IUCN Red List), but it may be declining in part of its impacts upon economic plants exploited by humans. range. Therefore, it becomes necessary to understand Indeed, the majority of the discussions held on the conservation status of species in different parts of parasitic plants in the literature have largely been their range. Hence, the International Union for focused on how best to eliminate them (McCallum Conservation of Nature developed guidelines to and Dobson, 1995). Parasitic plants are now being enable assessment at the regional and national levels. recognized as keystone species (Press and Phoenix, The present study has applied these guidelines in 2005). Notwithstanding the fact that they harm their identifying the conservation status of Thonningia host directly through parasitism, they offer other sanguinea in Southern Nigeria. ecological roles in the habitat such as maintaining community structure and evenness (Joshi et al., Thonningia sanguinea is a cryptic holoparasitic plant 2000), modifying the population dynamics, that is endemic to the tropical region of Africa. It is one of the few, if not, the only representative member vegetation zonation and nutrient cycling in forested of Balanophoraceae in Nigeria. It is a fleshy environments (Press and Phoenix, 2005) and dioecious herb growing from an underground tuber interactions with other trophic levels that include that forms bulb-like swellings at the points where it dispersers, pollinators, herbivores and fungal attaches to the roots of its host plants and it’s symbionts (Westbury and Dunnett, 2007). recognized by the above-ground inflorescence head. Thonningia sanguinea is used by the majority of the The IUCN Red List Categories and Criteria are used tribes in Southern Nigeria as a reliable traditional to assess the conservation status of wild species in remedy for many ailments (Imarhiagbe and sequence to objectively, ensure proper placement into a threat category based on the relative risk of Aigbokhan, 2019). Laboratory investigations about extinction (IUCN 2017). The IUCN Red List the plant have also revealed medicinal properties Categories and Criteria were initially developed to such as antibacterial activity (N'guessan et al., 2007), successfully assess extinction risk at the global level. antioxidant activity (Gyamfi et al., 1999), and the 160 Imarhiagbe and Aighokan Proceedings of 7th NSCB Biodiversity Conference, October 2020 effectiveness against the mycoses associated with HIV infection and AIDS (Ouattara et al., 2007). Substantial evidence suggests that T. sanguinea population is currently facing various threats in the wild. T. sanguinea is mostly found in forested environments. However, several studies have reported increasing habitat fragmentation and degradation. Despite the cultural relevance of T. sanguinea, current information on habitat characteristics, population size and distribution needed for assessing the conservation status in Nigeria are currently unavailable and/or the available ones are inadequate or insufficient. Using field surveys, this study assessed the conservation status of T. sanguinea as well as identify possible threats to its survival in Southern Nigeria. METHODOLOGY Population location: Thonningia sanguinea populations were located using meander searches, personal communications with the local people, and secondary data (Bullock, 1948; Otoide, 1982; Idu et al., 2002). Thonningia sanguinea populations were found in Cross River National Park in Cross River State, Okomu National Park in Edo State, Idanre and Ofosu Forest Reserves in Ondo State, Oban Hills Forest Reserve in Osun State, Omo Forest Reserve in Ogun State and Ehor Nu Wire, Okour, Okokhuo, and Iyanomo Community Forests in Edo State. Nigeria (Figure 1). Figure 1: Map of selected study sites in southern Nigeria Distribution: Two (2) reconnaissance studies were Sampling: To fully assess a detailed distribution, conducted to ascertain the presence and absence of T. stratified sampling method was used to locate sanguinea across the selected locations in southern populations of T. sanguinea in the selected locations Nigeria. Thematic maps delineating the distribution (Thorogood and Hiscock, 2007). Since individual T. were produced using ArcGIS 1.6 software and data sanguinea plants are difficult to distinguish due to the collected from the GPS readings of the selected hypogeic growth habit and ability to grow in tight clusters, the term ‘population’ refers to a close group locations. of one or more tubers appearing to have formed more Host identification: To identify the host plants, T. than one haustorium and/ or comprising of one or sanguinea tubers were excavated manually using a several individual plants. Thus, a 10 m x 10 m small shove. This was done to link the host-plant root quadrat was used to accommodate the number of host connection to a stem for ease of identification. The trees present in the study sites where data on host species were identified using appropriate population numbers were collected. identification guides (Hutchinson and Dalziel, 1968; Aigbokhan, 2014; Akobundu et al. 2016). 161 Imarhiagbe and Aighokan Proceedings of 7th NSCB Biodiversity Conference, October 2020 Determination of conservation status: The IUCN Red List Criteria at regional and national Levels (Ver. 4.0) was used to assess the conservation status of T. sanguinea in southern Nigeria (Table 1). Unlike the IUCN Red List Categories and Criteria, the guidelines for the application of IUCN Red List Criteria at regional and national level consist of eleven categories, namely Extinct (Ex), Extinct in the wild (EW), Regionally Extinct (RE), Critically Endangered (CR), Endangered (EN), Vulnerable (VU), Near Threatened (NT), Least Concern (LC), Data Deficiency (DD), Not Applicable (NA), and Not Evaluated (NE). Ethnoecological data: Due to anthropogenic disturbances, oral interviews were granted to the locals to determine the historical distribution, threats and local use(s) of T. sanguinea. A total of 104 persons comprising different individuals from Edo state, Ondo state, Cross River, Oyo state, Osun state, Ogun state, and Bayelsa state were interviewed in the course of the study. Overall, 78 (74%) were males and 24 (26%) were females. The occupations of the respondents were farming (89%), park ranger (2%), teaching (2%), and other unspecified occupations (8%). Table 1: Conservation status of Thonningia sanguinea using IUCN Red List Guidelines Criteria Is the taxon eligible for Red List assessment Can criterion A be applied? (Population reduction at a specific rate over 10 years or 3 generations (whichever is longer) in the past, present, and/or future) Can criterion B be applied? (Restricted geographic range and severe fragmentation, continuing decline and/or extreme fluctuations) Can criterion C be applied? (Small population size and continuing decline) Can criterion D be applied? (Very small or restricted population) Justification Conclusion 1) Description of the species was published by Vahl in 1810. Yes 1) The species was formerly believed to be very common in the past, but appears to be rare now. A few suitable breeding habitats are available due to the host dependence factor. No indication of the time period over which a presumed decline had taken place or data to be able to estimate the scale of population decline. No generation length available. NO Using a cell with of 2km, it was established that the Area of Occupancy (AOC) is 76.000 km2 while its Extent of Occurrence (EOC) is 37,076.228 km2 The population is fragmented in 21 locations which is greater than the threatened-status threshold of 10 There is no indication of a continuous decline or fluctuation in EOO or AOO, locations, and matured individuals NT No specified rate of a continuing population size decline Population size as estimated from the study, is about 49. Individual plant, may be inferred from the number of haustoria attachments which is currently inaccessible due to its subterranean nature. No specific of the number of matured individual given No indication of a continuous decline in the number of matured individuals. Based on the number of populations, it is likely to have more than 1000 matured individuals which exceeds the thresholds for CR, EN, and VU The population has an AOO of 76 km 2 which exceeds the thresholds for CR, EN, and VU Total number of locations amounted to 21, greater than the threshold for VU which is 5. No quantitative analysis has been carried out on T. sanguinea. NO 2) 3) 4) 1) 2) 3) 1) 2) 3) 4) 1) 2) 3) NT 1) Can criterion E be NO applied? (Quantitative analysis estimating probability of extinction in the wild) T. sanguinea was found not to qualify for any of the threatened categories that is Critically Endangered (CR), Endangered (EN) or Vulnerable (VU)). Presently, the conservation status of T. sanguinea in southern Nigeria is proposed as Near-threatened (NT). 162 Imarhiagbe and Aighokan Proceedings of 7th NSCB Biodiversity Conference, October 2020 comprised community and plantation forests. We recorded a total of 39 populations and 10 populations of T. sanguinea in the protected and unprotected sites respectively. From personal communications with the local people, T. sanguinea was believed to be very common and widespread in the past until recently when the species appear to be restricted only to a few forest relics. RESULT AND DISCUSSION The potential and confirmed distribution of Thonningia sanguinea in southern Nigeria is shown in Figure 2. In addition, a total of forty-nine (49) T. sanguinea populations were recorded in twenty-one (21) locations (Table 2). However, records obtained from the ethnoecological survey suggests a wider distribution including Delta, Bayelsa, Benue, and Taraba States in Nigeria. The host species supporting T. sanguinea populations in the study sites were fully matured trees comprising both native and exotic species (Table 2). Exotic host species such as Hevea brasiliensis (Euphorbiaceae) and Theobroma cacao (Malvaceae) were observed to support the parasite mainly in community and plantation forests whereas indigenous species such as Guarea cedrata (Meliaceae), Lophira alata (Ochanaceae), Musanga cecropiodes (Urticaceae), Myrianthus arboreus (Urticaceae), Ricinodendron heudelotii (Euphorbiaceae) were the hosts in natural vegetation. In addition, Figure 3 shows the occurrence of T. sanguinea in protected and unprotected sites of southern Nigeria. Protected sites includes National Parks and Forest Reserves while the unprotected sites Conversely, the threats to the survival of T. sanguinea populations in southern Nigeria include bushfire, forest degradation and herbivory. In this study, the respondents identified bushfire as the most dominant threat factor (Figure 4). This could have resorted to the destruction of host species and interrupt the haustoria connections with the host root. Also, the rate of forest degradation and habitat fragmentation have been on the increase in recent times. T. sanguinea is a holoparasitic species that rely solely on host species for survival (Otoide, 1982). Therefore a reduction in the population of potential hosts could lead to a reduction in the population of the parasite. Figure 2: Potential and confirmed distribution of Thonningia sanguinea in Southern Nigeria 163 Imarhiagbe and Aighokan Proceedings of 7th NSCB Biodiversity Conference, October 2020 Table 2: Host and number of Thonningia sanguinea in the selected locations in southern Nigeria State Study sites Status Host Coordinates *CROSS Cross River Protected Unknown 5.58972222° N RIVER 8.55500000° E *CROSS Cross River Protected Lophira alata 5.41444444° N RIVER 8.48388889° E *CROSS Cross River Protected Musanga cecropiodes 5.58972222° N RIVER 8.55500000° E *CROSS Cross River Protected Lophira alata 5.60694444° N RIVER 8.53055556° E *CROSS Cross River Protected Unknown 5.58972222° N RIVER 8.55500000° E **EDO STATE Ehor Nu Unprotect Hevea brasiliensis 6.39500000 °N Wire ed 5.96611111° E **EDO STATE Okokhuo Unprotect Musanga cecropiodes 6.81916667° N ed 5.71527778° E **EDO STATE Okour Unprotect Hevea brasiliensis, Musanga 6.45055556° N ed cecropiodes 6.32444444°E **EDO STATE Iyanomo Unprotect Hevea brasiliensis 6.35722222° N ed 5.81611111° E *EDO STATE Okomu Protected Ricinodendron heudelotii 6.43138889° N 5.43888889° E *EDO STATE Okomu Protected Musanga cecropiodes 6.45583333° N 5.56361111° E *EDO STATE Okomu Protected Myrianthus arboreus, Guarea 6.59361111° N cedreta 5.52361111° E *EDO STATE Okomu Protected M. cecropiodes, M. arboreus. 6.37083333° N 5.46388889° E *EDO STATE Okomu Protected Myrianthus arboreus 6.36722222° N 5.46055556° E *EDO STATE Okomu Protected Theobroma cacao 6.53222222° N 5.51305556° E ***ONDO Idanre Protected Theobroma cacao 7.28166667° N 5.39111111° E ***ONDO Ofosu Protected Musanga cecropiodes 6.79388889° N 5.35333333°E ***OSUN Oba hills Protected Unknown 7.82638889° N 4.32555556°E ***OYO IITA Protected Yet to be identified 7.71111111° N 4.03055556° E ***OYO IITA Protected Unknown 7.71111111° N 4.03055556° E ***OGUN Ijebu Ode Protected Unknown 6.869166° N 4.287415° E East *NP = National Park **CP = Community Forest ***FR = Forest Reserve 164 No. 4 3 2 2 2 3 3 2 2 2 3 2 2 2 1 2 3 2 3 2 2 Imarhiagbe and Aighokan Proceedings of 7th NSCB Biodiversity Conference, October 2020 80 40 Number of Respodents Number of T. sanguinea population 45 35 30 25 20 15 10 5 0 70 60 50 40 30 20 10 0 Unprotected forest Protected forest Forest ruminants Nature of the forest habitat Figure 3: Occurrence of Thonningia sanguinea in protected and unprotected sites of southern Nigeria Bushfire Unaware Figure 4: Ethnoecological perspective of the threats to T. sangiuinea in the wild the reproductive parts of the plant are the most obvious, hence a target for herbivores, which invariably hamper pollination, fruit formation, and dispersal. According to Webster and Parker, (2000), animals that feed on seeds, bulbs, or other reproductive parts directly reduce the plant’s reproduction and may kill the plant. Thonningia sanguinea has a penchant for disturbed areas of the forest, especially areas along forest margins and edges where sunlight penetrates to the ground (Imarhiagbe and Aigbokhan, 2019). Forest fragmentation increases the amount of edge within a plant community and thus making it easier for herbivores to penetrate into forest tracts for T. sanguinea inflorescence and this renders the population vulnerable (Fletcher et al., 2001). Aside the human-induced threats, destructive feeding habits on the inflorescence by insects and forest ruminants such as the slender mongoose (Galerella sanguinea) and the duiker Cephalophus sp. were also noted (Plate 1). These species cause significant damage to T. sanguinea populations in different forest habitats in southern Nigeria. Furthermore, Hofman and Roth (2000) reported Cephalophus maxwellii (Maxwell’s duikers) to feed heavily on T. sanguinea in the wild. The effects of herbivory on plants, especially small-sized ones could be catastrophic, depending on the part of the plant removed, the intensity of removal, and the timing of the attack relative to plant development (Fletcher et al., 2001). In the case of T. sanguinea, A A B B C C D D E E F F A-D: Forest ruminants feeding on T. sanguinea at Okomu National Park E-F: A caterpillar feeding and defecating on matured female inflorescence of T. sanguinea 165 Imarhiagbe and Aighokan Proceedings of 7th NSCB Biodiversity Conference, October 2020 brasiliensis. Indian Journal of Rubber Research, 15 (1) 33-35. Imarhiagbe, O. and Aigbokhan, E. I. (2019). Thonningia sanguinea Vahl. (Balanophoraceae) in Southern Nigeria: II. Patterns of genetic diversity and population structure within and between Populations. Makara Journal of Science, 23 (4): 193-203. IUCN, (2017). Guidelines for using the IUCN Red List Categories and Criteria. Version 13. The World Conservation Union, Switzerland: Prepared by the standards and Petition subcommittee. 108pp. Joshi, J., Matthies, D. and Schmid, B. (2000). Root hemiparasites and plant diversity in experimental grassland communities, Journal of Ecology, 88: 634-643. McCallum, H. and Dobson, A. (1995). Detecting disease and parasite threats to endangered species and ecosystems. Trends in Ecology and Evolution, 10: 190-193. N'guessan, J. D., Coulibaly, A., Ramanou, A. A., Okou, O. C., Djaman, A. J., and Guede-Guina, F. (2007). Antibacterial activity of Thonningia sanguinea against some multi-drug resistant strains of Salmonella enterica. African Health Sciences, 7 (3): 155-158. Otoide, V. O. (1982). Thonningia sanguinea- a new parasite on rubber roots. Tropical Pest Management, 28 (2): 186 - 188. Ouattara, B., Kra, A. M., Coulibaly, A. and GuedeGuina, F. (2007). Efficiency of ethanol of Thonningia sanguinea against Cryptococcus neoformans. African Health Sciences, 17 (4): 219–22. Press, M. C. and Phoenix, G. K. (2005). Impacts of parasitic plants on natural communities, New Phytologist, 166 (3): 737-751. Thorogood, C. J. and Hiscock, S. J. (2007). Host specificity in the parasitic plant Cytinus hypocistis. Research Letters in Ecology, 84234: 1-4. Webster, C.R. and Parker, G.R. (2000). Evaluation of Osmorhiza claytonia (Michx.) C. B. Clarke, Arisaema triphyllum (L) Schott, and Actaea pachypoda Ell. as potential indicators of whitetailed deer over- abundance. Natural Areas Journal, 20:176–187. Westbury, D. B. and Dunnett, N. P. (2007). The impact of Rhinanthus minor in newly established meadows on a productive site. Applied Vegetation Science, 10: 121 - 129. CONCLUSION AND RECOMMENDATION This study identified the host species and locations of T. sanguinea populations in southern Nigeria. Bushfire, forest degradation and herbivory were identified as major threats. Applying the IUCN guidelines, the conservation status of T. sanguinea in southern Nigeria could be described as nearthreatened. However, if the current level threats, especially by fire continues, the species T. sanguinea could qualify for any of the threatened categories in the near future. Presently, the mechanism of domestication is still far-fetched. It is recommended, therefore, that the identified T. sanguinea populations from this study should be protected and allowed to proliferate with the host plant species. FUNDING STATEMENT This project was funded by the TETFUND 20172018 (Batch 12th) Research Project Intervention. REFERENCES Aigbokhan, E. I. (2014). Annotated checklist of vascular plants of Southern Nigeria: A systematic approach. Benin City, Nigeria: Uniben Press. 346pp. Akobundu, I. O., Ekeleme, F., Agyakwa, C.W. and Ogazie, C.A. (2016). A handbook of West African weeds. Ibadan, Nigeria: International Institute of Tropical Agriculture. 381pp. Bullock, A. A. (1948). Thonningia Vahl. Kew Bulletin, 3 (3):363-367. Fletcher, D. J. Shipley, L. A. McShea, W. J. and Shumway, D. L. (2001). Wildlife herbivory and rare plants: the effects of white-tailed deer, rodents, and insects on growth and survival of Turk’s cap lily. Biological Conservation, 101: 229-238. Gyamfi, M. A., Yonamine, M. and Aniya, Y. (1999). Free-radical scavenging action of medicinal herbs from Ghana: Thonningia sanguinea on experimentally-induced liver injuries. General Pharmacology, 32 (6): 661-667. Hofman, T. and Roth, H. (2000). Feeding preferences of duiker (Cephalophus maxwell, C. Rufilatus and C. Niger) in Ivory Coast and Ghana. Mammalian Biology, 68: 65-77. Hutchinson, J. and Dalziel, J. M. (1968). Flora of West Tropical Africa. London, England: Crown Agents for Overseas Governments and Administrations.276pp. Idu, M., Begho, E. R. and Akpaja, E. O. (2002). Anatomy of attachment of the root parasite Thonningia sanguinea Vahl.on Hevea 166