Nrican Invertebrates African Invertebrates 66(1): 1-18 (2025) DOI: 10.3897/Afrinvertebr.66.138662 Research Article Active restoration of post-mining forest benefits the activity density, but not the diversity of spider communities across the seasons in Ghana Harriet Kinga’, Frederick Gyasi Damptey2® Danilo Harms®®, Rudy Jocqué*®, Arnaud Henrard*®, Klaus Birkhofer' ee wo NY — Department of Ecology, Brandenburg University of Technology Cottbus-Senftenberg (BTU), Cottbus, Germany Forest Aid Ghana, P.O. Box KN 6218, Kaneshie-Accra, Ghana Museum of Nature Hamburg - Zoology, Leibniz Institute for the Analysis of Biodiversity Change (LIB), Hamburg, Germany Royal Museum of Central Africa, Tervuren, Belgium Corresponding author: Harriet Kinga (harrietkinga@gmail.com) OPEN Qaccess This article is part of: Gedenkschrift for Prof. Stefan H. Foord Edited by Galina Azarkina, Ansie Dippe- naar-Schoeman, Charles Haddad, Robin Lyle, John Midgley, Caswell Munyai Academic editor: John Midgley Received: 5 October 2024 Accepted: 21 November 2024 Published: 10 Junuary 2025 ZooBank: https://zoobank. org/7B641FB8-8150-47ED-A289- DASDBESEB563 Citation: Kinga H, Damptey FG, Harms D, Jocque R, Henrard A, Birkhofer K (2025) Active restoration of post- mining forest benefits the activity density, but not the diversity of spider communities across the seasons in Ghana. African Invertebrates 66(1): 1-18. https://doi.org/10.3897/ Afrinvertebr.66.138662 Copyright: © Harriet Kinga et al. This is an open access article distributed under terms of the Creative Commons Attribution License (Attribution 4.0 International - CC BY 4.0). Abstract Forest restoration often involves monitoring programmes to determine whether biodi- versity levels and ecosystem services have changed over time. This study investigated changes in ground-hunting spider communities (families Ctenidae, Lycosidae and Zo- daridae) in an actively restored forest, an unrestored gravel mine, and two alternative land-use types (agroforestry system and an arable field) to assess whether a two-de- cade post-mine restoration programme has been successful in restoring biodiversity to levels of a reference natural forest. The overall activity density of ground-hunting spiders (based on both juveniles and adult specimens) was highest in the natural and the re- stored forest in the dry season and lowest in the arable field and agroforestry system in the wet season. The inverse Simpson index was highest at the gravel site in the wet sea- son, followed by natural forest in both seasons and lower values in the restored forest. The community composition of spiders differed significantly between land-use types (open versus forest habitats) and the interaction between land use and season also differed significantly. The species Pardosa injucunda and Trochosa gentilis dominated the communities in the restored forest, but Africactenus monitor dominated the natural forest and Hogna gratiosa dominated communities in the gravel site. Surprisingly, active forest restoration promoted the activity density of ground-hunting spiders displaced by mining activities to levels even higher than in the reference natural forest after two de- cades. However, the community composition of the restored forest was more similar to the agroforestry system than to the natural forest. These results highlight the benefits of restoring former mining sites but also show the trade-offs in terms of restoration goals, as natural forest biodiversity of spiders was not achieved after 20 years. Key words: Agroforestry system, Araneae, biodiversity conservation, community com- position, deforestation, mining Harriet Kinga et al.: Active restoration of post-mining forest across seasons in Ghana Introduction Global deforestation rates continue unabated, with the majority of deforesta- tion occurring in tropical regions that are home to primary forests and rich in biodiversity (Ritchie et al. 2021). According to the Global Forest Resource Assessment, the world has lost approximately 420 million hectares of forest since 1990 (FAO and UNEP 2020). In Ghana, deforestation rates are particularly high, estimated at 3.5 percent of the total forest area per year, equivalent to 315,000 hectares (World Bank 2020). Agricultural land use, logging, mining, and infrastructure development are the main drivers of deforestation, often leading to ecological imbalances with significant biodiversity and societal impacts in Ghana (Damptey et al. 2021; Abugre and Sackey 2022; Asare et al.2022; Ben- tsi-Enchill et al. 2022) and worldwide (Hansen et al. 2010; Foord et al. 2020; Fitzgerald et al. 2021; Masolele et al. 2024). Several local and international ini- tiatives have been introduced to address forest loss in Ghana including refor- estation and sustainable land management practices, which aim to reduce for- est degradation while restoring degraded ecosystems to support biodiversity and society (Damptey et al. 2021; Kumi et al. 2024). Both passive (unassisted) and active restoration programmes, such as planting tree seedlings, focus on restoring biodiversity while also providing ecosystem goods and services to local human communities (Damptey et al. 2020). Effective monitoring of res- toration programmes is an important tool for evaluating outcomes and adjust- ing or revising restoration strategies, to achieve long-term conservation goals (Hansen et al. 2010; Bullock et al. 2011). Historically, restoration monitoring in Ghana has often focused on the use of a few indicators such as tree species composition and diversity (Nero 2021) or soil attributes (Damptey et al. 2020; Brown et al. 2024), with little focus on arthropod biodiversity and their important contributions to ecosys- tem functioning (Birkhofer et al. 2024; Cardoso et al. 2024). The few studies to date that have included arthropods in their forest restoration monitoring programmes in West Africa have focused on higher taxonomic levels (e.g., order or family classification: Kyeremanten et al. 2020; Damptey et al. 2023). Taxonomic surrogacy addresses time and resource limitations and is often sufficient in ecological research due to comparable habitat requirements of species within families or genera (taxonomic sufficiency: Birkhofer et al. 2012). However, results from such approaches may still suffer from the lack of species-level identification, as species within a higher taxonomic group of- ten have different ecological traits and may therefore respond differently to changes in habitat conditions (Ong and Hamid 2022). For a holistic view of the performance of restored ecosystems in terms of arthropod biodiversity recovery, the use of species levels in ecological monitoring programmes is therefore beneficial. Here, we focus on spiders (Arachnida, Araneae) and their potential role as indicators of restoration success. Spiders are the dominant predators in ter- restrial arthropod food webs (Potapov et al. 2022) and provide essential eco- system services including provisioning (e.g., providing venom for the pharma- ceutical industry), regulating (pest control and invasive species management; Dippenaar-Schoeman et al. 2005), supporting (nutrient cycling), and cultural and spiritual (e.g., providing a sense of place) services (Cardoso et al. 2024). African Invertebrates 66(1): 1-18 (2025), DOI: 10.3897/Afrinvertebr.66.138662 2 Harriet Kinga et al.: Active restoration of post-mining forest across seasons in Ghana Changes in spider populations can also indicate shifts in insect populations, which are essential for ecosystem functioning (Marc et al. 1999). Spiders are an important food source for a variety of other organisms, including birds, small mammals and other arthropods, contributing to the overall biodiversity of the ecosystem (Marc et al. 1999). They also serve as bio-indicators for ecological monitoring due to their sensitivity to environmental changes caused, for exam- ple, by pollution, habitat modification or climate change (Jocqué et al. 2005; Nyffeler and Birkhofer 2017). Among spiders, some taxa are known to be restricted to more open hab- itats such as Lycosidae Sundevall, 1833 (Jocqué and Alderweireldt 2006; Juakaly and Jocqué 2021) while others, such as some Ctenidae Keyserling, 1877 (Steyn et al. 2003; Jocqué et al. 2005; Henrard and Jocqué 2017) and the Zodariidae Thorell, 1881 (Jocqué 1993; Nzigidahera et al. 2011; Dankittipa- kul et al. 2012), are characteristic of tropical forests. These taxonomic groups are therefore ideal for studying the impact of deforestation and monitoring habitat restoration. We therefore studied ground-hunting spider communities of the families Ctenidae, Lycosidae, and Zodariidae in an unrestored and re- stored gravel mine site 20 years after restoration to determine the restoration trajectory compared to a reference natural forest and two alternative land uses (arable field and agroforestry system) in the dry and wet seasons. Specifical- ly, we investigated how land use and seasonality affected the activity density and species composition of spider communities. We also analysed whether individual spider species preferred certain land-use types or showed a strong seasonality, which might indicate their suitability as indicator species for res- toration stages and success. Methodology Study site The study was conducted in Ghana in the Ahafo region (Fig. 1), which is char- acterised by semi-deciduous forest (SDFZ), an average annual rainfall between 900 and 1,500 mm, and an average daily temperature of 25 °C. This region is characterised by two distinct seasons: the hot dry harmattan (November to March) and the rainy season (April to October) (Damptey et al. 2020). The Bo- somkese Forest Reserve (agroforestry system; AS) is located in the semi-de- ciduous south eastern forest zone and is situated at 7°6.338'N, 2°14.782'W. The Asukese Forest Reserve (primary natural forest; NF) is located in the humid semi-deciduous north western forest zone at 7°8.469'N, 2°31.107'W. The Terchire Restoration Area (restored forest; RF), which covers an area of 15.4 ha (2°10.842'N, 7°14.075'W), was exploited for gravel for road con- struction until 1998 and was actively restored in 1999 by planting indigenous and fast-growing exotic nitrogen-fixing tree seedlings (Damptey et al. 2020). The gravel site (GS) covers an area of approximately 4 ha and is located 1.8 km (7°14.150'N, 2°9.602'W) from the RF (Fig. 1). The GS has been aban- doned since 1995 and is colonised by a few shrubby plants (Chromolaena odo- rata and Pennisetum purpureum). The arable field (AF) is located around the RF and is cultivated with maize, plantain, cassava and cocoa, among others (Damptey et al. 2020). African Invertebrates 66(1): 1-18 (2025), DOI: 10.3897/Afrinvertebr.66.138662 3 Harriet Kinga et al.: Active restoration of post-mining forest across seasons in Ghana Tamale . Akrodie Kumasi e 0 50 86100 200 0 25 50 ES Kilometers ——= Kilometers 0 014 0.2 0 005 0.1 EES Kilometers a) Kilometers Figure 1. Map of Ghana (1) showing the Ahafo Region (2) and the studied land-use types (A Asukese Forest Reserve - Natural Forest - NF B Bosomkese Forest Reserve — Agroforestry System - AS C Restored Forest - RF D Arable Field -AF E Gravel Site-GS). Sampling design The five land-use types were studied in both seasons (dry and wet) using eight replicated 20 x 20 m plots, resulting in 40 study plots across the five land uses. Ground spider communities were sampled continuously, with five pitfall traps on each plot emptied weekly for 10 weeks in each sampling season. The first sampling campaign was conducted in the dry season (January to March 2019), followed by a rainy season campaign (June to August 2019). Pitfall traps were filled with a 50:50 mixture of ethylene glycol and water, and all pitfall traps were covered with small roofs to prevent the dilution of the trapping fluid by rain (Un- derwood and Quinn 2010). Pitfall trap samples were stored in 70% ethanol and later sorted into taxonomic groups (order, suborder or family) according to avail- able identification keys for spiders (Dippenaar-Schoeman and Jocqué 1997). Sample identification In West Africa, most spider species have yet to be described, making it difficult to identify adults to species level due to the lack of taxonomic keys. To over- come this obstacle, the limited literature available (Roewer 1959; Henrard and African Invertebrates 66(1): 1-18 (2025), DOI: 10.3897/Afrinvertebr.66.138662 4 Harriet Kinga et al.: Active restoration of post-mining forest across seasons in Ghana Jocqué 2017) was used to place some adults in the correct morphospecies. For others with insufficient or unavailable literature, further species identifi- cation was achieved through museum visits to the Royal Museum for Central Africa (RMCA), Tervuren, Belgium, and the Naturmuseum Senkenberg (SMF), Frankfurt, Germany. During these visits, complete identification of adult Cteni- dae specimens to species level was achieved and many juveniles could be as- signed to a specific genus. Most of the Lycosidae were identified as species by first examining the original taxonomic literature, followed by the examination of the original type specimens at the SMF (Roewer 1959). Only one species of Zodariidae could be identified to species level. The remaining six species (Appendix 2) were given provisional morphospecies codes as they represent undescribed species. Data analysis The overall activity density of spiders was based on the total catch of both juvenile and adult spiders in the families Ctenidae, Lycosidae and Zodariidae. The multivariate species composition of ground-hunting spider community fo- cused only on the composition of identified species in these three families. The multivariate species composition of spider communities in different land uses and seasons, as well as the interaction term between land use and the season, was analysed using permutational multivariate analysis of variance (PERMANOVA) based on log(x+1) transformed activity densities of all species from the selected families and Bray-Curtis similarities (Clarke et al. 2014) and an unrestricted permutation of the raw data with 9999 permutations was ap- plied (Anderson 2008). Land-use types (5 levels) and seasons (2 levels) were both used as fixed factors, and plots (8 levels) nested within the land-use types were used as random factors to reflect the repeated measures design. In case of statistically significant differences for a fixed factor, pairwise post-hoc tests were carried out for pairs of levels of factors and were performed using PER- MANOVA. The same model was used to analyse the log(x+1) transformed over- all activity density (the total number of ground-hunting spiders) and the inverse Simpson index based on Euclidean distances in each land use and for the three families. Non-metric multidimensional scaling (NMDS) ordination based on Bray-Curtis similarities was used to indicate the similarity between samples within and between plots of different land-use types and the goodness of fit of NMDS ordinations was assessed based on the 2-D stress value (Clarke et al. 2014). A similarity percentage analysis (SIMPER) was used to identify char- acteristic species for each land use and season, based Bray-Curtis similarities and a 70% cut-off for total contribution (Somerfield and Clarke 2013). Results A total of 1852 individual spiders from five land-use types (natural forest, agro- forestry system, restored forest, arable field and gravel sites) and across two seasons (wet and dry) were identified in the three families. A total of 29 spe- cies, comprising 804 males, 397 females and 651 juveniles were identified from the following families: Ctenidae (7 species), Lycosidae (12) and Zodariidae (7) (Appendix 1). African Invertebrates 66(1): 1-18 (2025), DOI: 10.3897/Afrinvertebr.66.138662 5 Harriet Kinga et al.: Active restoration of post-mining forest across seasons in Ghana Activity density and inverse Simpson index The overall activity density of spiders differed significantly between land uses and seasons, and the interaction term between land uses and seasons was also significant (Table 1A). The overall activity density was highest in the re- stored forest followed by the natural forest (Fig. 2A). The overall activity density was higher in the dry season than in the wet season. The overall activity density of spiders was higher in the restored forest in both seasons and in the natural forest in the dry season than in the other land uses. The restored forest had the highest activity density in the dry season and the arable field had the lowest activity density in the wet season. The inverse Simpson index differed significantly between land uses, but not between seasons and the interaction term between land uses and seasons was significant (Table 1B). The inverse Simpson index was highest on the gravel site in the wet season, followed by the gravel site in the dry season and the natural forest in both seasons (Fig. 2B). The inverse Simpson index was lowest in the arable field in both seasons and in the agroforestry system in the wet season. Species composition across habitats and seasons The species composition of spider communities differed between land-use types but not between seasons and the interaction term between land uses and season was also significant (Table 1C). The NMDS ordination shows dissimi- larities between spider communities in the different land uses and followed a Table 1. PERMANOVA results for the effect of the land use and season on the A) overall activity density, B) inverse Simpson index (Hill number 2) and C) multivariate species composition of spider communities (df: degree of freedom; SS: sum of squares, MS: mean sum of squares, Pseudo-F: F value by permutation, P(perm): P-values based on 9999. Significant effects are in bold. A) Activity dens. df Ss Ms Pseudo-F P(perm) Plot a0 4257.90 12165 1.64 0.072 Land use 4 6057.3 1514.3 12.448 0.001 Season 1 806.45 806.45 10.844 0.002 Land-use x Season 4 907.68 226.92 3.0513 0.031 Res 35 2602.9 74.368 Total 79 14632 B) Inv. Simpson df Ss MS Pseudo-F P(perm) Plot a5 24.76 0.71 0.66 0.890 Land use 4 47.79 11.95 16.89 0.001 Season 1 0.24 0.24 0.22 0.639 Land-use x Season) 4 12.50 3.12 2.91 0.037 Res 35 37.64 1.08 Total 79 122.91 C) Species comp. | df Ss Ms Pseudo-F P(perm) Plot a5 50118.00 1431.90 1.35 0.016 Land use 4 78157.00 19539.00 t3.65 0.001 Season 1 2235.60 2235.60 2.10 0.059 Land-use x Season) 4 8211.40 2052.80 1.93 0.008 Res 35 37175,00 1062.10 Total 79 175900.00 African Invertebrates 66(1): 1-18 (2025), DOI: 10.3897/Afrinvertebr.66.138662 Harriet Kinga et al.: Active restoration of post-mining forest across seasons in Ghana Activity density Inverse Simpson index (Hill Number 2) Figure 2. Overall activity density (A) and inverse Simpson index (B) (Hill number 2) of spiders for interactions between land-use types (NF, natural forest; AS, agroforestry system; AF, arable field; GS, gravel site; and RF, restored forest) and sea- son (W, wet; D, dry). Single points indicate outliers based on the Median and Interquartile Deviation Method (IQD), the hor- izontal line is the median, boxes are 25" and 75" percentiles and whiskers show the 90" and 10" percentile respectively. gradient from the gravel site through the arable field, agroforestry system and restored forest to the natural forest (Fig. 3). Spider communities in the agrofor- estry system overlapped with those in the restored forest. Communities in the restored forest differed by 64% from the arable field with Amicactenus eminens (Arts, 1912), Africactenus monitor (Steyn & Jocqué, 2003), Mallinella sp3, and Pardosa injucunda (O. Pickard-Cambridge, 1876) having higher activity densities in the restored forest and with Anahita lineata (Simon, 1897) only present in the restored forest, but absent in the arable field. Furthermore, the communities in the restored forest differed by 68% from the gravel site with Mallinella sp3, P. injucunda and Trochosa gentilis (Roewer, 1960) having higher activity densities in the restored forest (Fig. 4). Similarly, Hogna duala (Roewer, 1959), Hogna gratiosa (Roewer, 1959), and Mallinella banda- maensis (Jézéquel, 1964) had higher activity densities in the gravel site, while Mallinella sp3 was only present in the restored forest but not in the gravel site. Spider community composition differed by 68% between the restored forest and the gravel site, but the differences were mainly driven by the activity densi- ties of the seven most common species. Higher activity densities of Mallinella sp3, P. injucunda, and T. gentilis were observed in the restored forest than in the gravel site while M. bandamaensis, H. gratiosa, H. duala, and Hippasosa pilosa (Alderweireldt, 1996) had higher activity densities at the gravel site. Communi- ties in the reference natural forest differed by 61% from the restored forest with A. eminens, A. monitor, Mallinella sp1, Mallinella sp3 and having higher activity densities in the natural forest, and A. lineata, present only in the restored but not in the natural forest. Species composition of spider communities only showed a statistical trend for differences between the wet and dry seasons and with the wet season char- acterised by higher activity densities of H. duala, H. gratiosa, P injucunda, and T. gentilis (Fig. 5A—D). African Invertebrates 66(1): 1-18 (2025), DOI: 10.3897/Afrinvertebr.66.138662 7 Harriet Kinga et al.: Active restoration of post-mining forest across seasons in Ghana 2D Stress: 0.2 A Natural forest W Agroforestry system Arable field ©} Gravel site © Restored forest Figure 3. Non-metric multidimensional scaling (NMDS) ordination based on log-transformed (log(x+1)) activity densities of spider species and Bray-Curtis similarities between plots of different land-use types. The 2-d stress value is 0.2. Aj Africactenus monitor B] Hogna gratiosa > > = ra w 7) Cc c ® o a2) a2) = = 2 5 o xe) x 77) 7) Cc = i) o TC ao) 2 ry = 2 xe) rs) 1s) is) <