Diet Composition of the Common African Toad, Sclerophrys Regularis (Anura: Bufonidae), in a Human-Modified Landscape

Herpetology Notes, volume 14: 1167-1176 (2021) (published online on 01 September 2021)

Diet composition of the Common African Toad, Sclerophrys regularis (Anura: Bufonidae), in a human-modified landscape

Benjamin Yeboah Ofori1,*, John Bosu Mensah1, Roger Sigismund Anderson2, Jones Kpakpa Quartey3, and Daniel Korley Attuquayefio1

Abstract. The Common African Toad, Sclerophrys regularis, is widespread and common in West Africa, yet little is known about its ecology and natural history. Here, we assessed the dietary composition and trophic niche breadth and overlap of S. regularis in human-modified landscapes in Accra, Ghana, using gut content analysis. Our investigation of 74 individual toads from farmland and developed urban areas found 935 prey items from six invertebrate classes (Arachnida, Chilopoda, Diplopoda, Gastropoda, Insecta, and Polychaeta; comprised of at least 18 orders and 31 families). Hymenoptera (family: Formicidae) and Coleoptera were the most consumed prey items. We found a high degree of dietary niche overlap between males and females, suggesting no obvious sex-specific preferences in diet. Generally, a positive, but statistically insignificant correlation existed between snout-vent length of toads and the diversity and quantity of consumed prey items. The broad dietary niche of S. regularis suggests this toad is a generalist arthropod predator. Our findings highlight basic aspects of the ecology of S. regularis, which we hope can be used to inform conservation and management strategies for the species.

Key words. Amphibians, Natural history, Predator, Trophic niche, Urbanisation

Introduction environmental changes (Hof et al., 2011), there remains substantial knowledge gaps in our understanding of the Amphibians are among the most species-rich groups ecology and basic biology of many tropical amphibians, of terrestrial vertebrates, with hundreds of new species particularly in urban landscapes (Hamer and McDonnell, still being discovered annually (Pincheira-Donoso et 2008). This knowledge gap, if not bridged, could hinder al., 2013). They are important components of tropical the conservation of tropical amphibians. ecosystems, influencing food webs and energy flow by The dietary niche of amphibians is an important aspect their feeding behaviour (Le et al., 2018) and by serving of their natural history and determines many of their as prey for numerous vertebrates (Gibbons et al., interactions within the environment (Alveal and Diaz- 2006). Yet, amphibians are one of the most threatened Paez, 2021). Amphibian trophic interactions are essential vertebrate taxa worldwide (Stuart et al., 2004), with over components of food web structure and provides insight 30% of all amphibian species threatened (Baillie et al., into their population dynamics as well as the selective 2004) in part due to their high susceptibility to habitat pressure they may be exerting on their prey (Layman modifications, invasive species, overexploitation, et al., 2015). Access to high quality food promotes the climate change and infectious disease (Stuart et al., success of amphibians because it can influence their 2004; Cushman, 2006; Pound et al., 2006; Leduc et physiology, body condition, and fitness (Scholz et al., al., 2012; Scheele et al., 2019). Despite their ecological 2020). Conversely, limited food availability can reduce importance and high vulnerability to climate and other reproductive success and survival rate, ultimately altering their population dynamics (Scholz et al., 2020). Furthermore, as there can be a direct relationship between habitat condition and prey availability, abundance, and 1 Department of Animal Biology and Conservation Science, University of Ghana, Legon, Ghana. distribution, the dietary patterns of amphibians can be 2 African Regional Postgraduate Programme in Insect Science, used to inform conservation and management strategies University of Ghana, Legon, Ghana. (Bastista et al., 2011). 3 Centre for African Wetlands, University of Ghana, Legon, The Common African Toad, Sclerophrys regularis Ghana. (Reuss, 1833) (Amphibia: Bufonidae), is a large * Corresponding author. E-mail: [email protected] sexually dimorphic toad (adult females = 70–130 mm © 2021 by Herpetology Notes. Open Access by CC BY-NC-ND 4.0. snout-vent length [SVL] and males = 62–91 mm; Rödel 1168 Benjamin Yeboah Ofori et al.

2000) with rugose skin and a dark olive-brown dorsal and is a good source of protein in many parts of Nigeria, surface, a white to beige underside, and a distinguishing Burkina Faso, and northern Ghana (Akinsanya et al., black gular patch for males (Deef, 2019). This species 2020). Yet despite it being widespread and common, is widely distributed in Sub-Saharan Africa (Iyaji et al., there is still much to learn about its basic ecology and 2015; Channing and Rödel, 2019), with its latitudinal life history. Indeed, there is a paucity of information on distribution ranging from northern Egypt to north-western the dietary patterns of S. regularis. To help bridge this Angola and its longitudinal distribution extending from knowledge gap, we assessed the trophic niche pattern Senegal to Ethiopia (IUCN SSC Amphibian Specialist of S. regularis in human-modified landscape (i.e., Group, 2016; Channing and Rödel, 2019). The species farmland and urban area) in Accra, Ghana. Specifically, is adapted to a variety of habitats, including forest we assessed diet composition, trophic niche breadth, margins, moist and dry savannah, agricultural areas, and dietary overlap, as well as the relationship between and other habitats associated with rivers (Deef, 2019) SVL of toads and diversity of consumed prey items.

Figure 1. Study area on the University of Ghana’s Legon Campus showing the developed urban area (shaded in yellow) and farmland (shaded in lime green) where Common African Toads, Sclerophrys regularis, were collected. Diet composition of the Common African Toad in a human-modified landscape 1169

Materials and Methods Crops grown in the farm include mango, cashew, maize, and vegetables. Study Area. The study was conducted on Legon Data Collection. Using visual encounter surveys, Campus (5.6508˚N, 0.1869˚W) of the University of samples were collected from farmland (Fig 2A, B) and Ghana (Fig. 1). The campus has a total area of 1300 developed areas on the University of Ghana, Legon hectares (13 km²) and is located about 13 km north- east of Accra, the capital city of Ghana (Gbogbo et Campus (Fig. 2C, D). Prior to sampling, the study al., 2017). The climate of the area is characterised by area was surveyed and the breeding sites of toads were a pronounced gradient of mean annual rainfall ranging determined using points of male calls. Samples were from 733–1118 mm distributed over a major (May– collected from July to September between the hours of July) and minor (September–October) rainy season and 22:00 GMT and 08:30 GMT. During the early hours of a daily mean temperature of about 30 °C (Gbogbo et al., the morning, toads were searched for under leaf litter, 2017). The vegetation is generally coastal grasslands, fallen logs, rocks, and other microhabitats where toads thickets, and dry forest (Garshong et al., 2013), with are known to seek refuge. During chorusing nights, most of the natural vegetation converted into developed calling males or pairs in amplexus were captured by hand areas (e.g., buildings, markets, roads, and other man- following Quiroga et al., (2015) and Oropeza-Sanchez made infrastructure) and farmland. The only remnant et al. (2018). The sexes of individuals were determined of the original vegetation is within the Legon Botanical using the presence or absence of sub-gular pigmentation Garden, which is located north of the campus and (Vera-Candioti et al., 2019). The SVL of individuals covers an area of about 2.0 km2. The developed urban was measured using Digital Vernier callipers (+/- 0.01 area, which covers about 7.3 km2, includes areas mm). The toads were sacrificed humanely according around students’ halls, hostels, chalets, staff bungalows, to international standards by euthanising them with academic facilities, central administration blocks, Xylocaine. They were then dissected and their stomach library block, bookshops, banking square, restaurants, contents were emptied into petri dishes containing and canteens. The farmland is located adjacent to the 70% ethanol. With the help of a dissecting microscope, botanical garden and covers an area of about 1 km2. invertebrates in the stomach content were identified to

Figure 2. Typical habitat types in the farmland (A and B) and developed urban areas (C and D- drains behind man-made structures) where Common African Toads, Sclerophrys regularis, were captured. Photos by John Bosu Mensah. 1170 Benjamin Yeboah Ofori et al. the highest taxonomic level possible (order or family) respectively (Table 1). Of the non-insect orders, following the identification keys by Triplehorn and Polychaetes were the most frequent prey category, Johnson (2011). Approval for the present study was occurring in 50% of individuals with gut content, granted by the University of Ghana College of Basic followed by Arachnids (25%) and Chilopods (21.4%). and Applied Sciences Animal Care and Research Ethics For the class Insecta, the prey category with the highest Committee (Ref. No. ECBAS 024/18-19). frequency of occurrence was Hymenoptera, followed Data Analysis. We calculated the Numerical by Coleoptera and Orthoptera (Table 1). Percentage (N%) as (Ni/Nt) x 100, where Ni is the In the developed urban area, a total of 507 prey number of prey items in any prey category (i) and Nt is items, comprising six invertebrate classes (Arachnida, the total number of all prey categories. The Frequency Chilopoda, Diplopoda, Gastropoda, Insecta, and of Occurrence (F%) was estimated as the number of Polychaeta) from at least 15 orders and 28 families toad stomachs in which category i prey were found. The were obtained from the toads’ gut contents. Once again, trophic niche breadth was estimated using the Shannon- the class Insecta formed the majority (91.7%) of all the Wiener index H’ as -∑ [(pi) ×ln (pi)], where ‘pi’ represents prey items, with Hymenoptera (74.0%) and Coleoptera the proportion of total abundance represented by the ith (10.1%) being the most numerically abundant (Table species (any individual member of the prey categories in 2). Formicidae was the most abundant family (74.0%), the stomach content). A Sorenson’s similarity index was and the most consumed prey category with 91.1% of used to assess the dietary niche overlap between sexes. individuals with prey within their gut contents. We used Pearson’s correlation coefficient (r) to assess Comparison between males and females. In general, the correlation between (1) SVL and prey diversity there was no significant difference in terms of the (richness) and (2) SVL and prey category abundance. A frequency of occurrence of the different prey categories chi-square test was used to assess the significance of the between males and females (Table 3). However, differences in frequency of occurrence and numerical frequency of occurrence of Coleoptera and Diplopoda abundance of consumed prey items between males was significantly higher in females than males from and females. All analyses were done in the R software the urban area (χ2 = 6, p = 0.01). Also, the frequency (Version 4.0.5) and significance was set at an alpha level of occurrence of Chilopoda was significantly higher of 0.05. (χ2 = 6.43, p = 0.01) in females than males from the farmland. In terms of the numerical abundance of the Results prey items, female toads consumed significantly higher Abundance, diversity, composition, and frequency quantity of the prey categories Chilopoda, Coleoptera, of occurrence of prey items. A total of 44 individual Diptera, Hymenopera, Orthoptera, and Polychaeta (4.26 toads (n = 23 females, n = 21 males) and 48 (n = 19 ≤ χ2 ≥ 40.76, p ≤ 0.04; Table 3). The female toads from females, n = 29 males) were captured from the farmland the farmland consumed at least 15 prey items, while and developed urban area, respectively. The proportion males consumed nine prey items, with all the orders of individuals with empty stomachs was 34.1% in the of prey items found in males being present in females. farmland and 6.3% from the developed urban area. Of Therefore, females had a slightly higher niche breadth the individuals with stomach content in the farm land, (H’ = 1.905) than their male counterpart (H’ = 1.627). In 19 were females and 10 were males, whereas in the the urban area, females had a higher niche breadth (H’ developed urban area, 16 were females and 29 were = 1.364) than males (H’ = 0.894), but males consumed males. a slightly higher variety of prey items and significantly A total of 428 prey items, consisting of six invertebrate greater quantities of Hymenoptera (χ2 = 116.48, p ≤ classes (Arachnida, Chilopoda, Diplopoda, Gastropoda, 0.0001) and Polychaeta (χ2 = 6.26, p = 0.01; Table 3). Insecta, and Polychaeta) and belonging to at least The dietary niche overlap between males and females 16 orders and 31 families, were found in toads from at both the farmland (Sorenson’s index = 75%) and farmland. The majority (88.8%) of these were developed urban area (Sorenson’s similarity index = arthropods, of which 82.5% were insects. The most 80%) was high. abundant prey items were from the order Hymenoptera Correlation between SVL and diversity and (39.5%), Coleoptera (15.7%), and Diptera (12.9%). abundance of prey items. In both developed urban Formicidae and Stratiomyidae were the most abundant area and farmland, we found a positive, but statistically insect families, with 38.6% and 11.4% of prey items, insignificant correlation between SVL and diversity Diet composition of the Common African Toad in a human-modified landscape 1171

Table 1.Table Taxonomic 1. Taxonomic composition composition of prey of prey items items (n (=n 428)= 428) found found in in stomachsstomachs ofof CommonCommon African African Toads, Toads, Sclerophrys regularis, from theSclerophrys farmland regularisat the University, from the of farmland Ghana’s at Legonthe University Campus of ( nGhana’s = Number Legon of Campusitems, N% (n = = Number Numerical of items, percentage, N% = F = frequency of occurrenceNumerical and percentage, F% = percentage F = frequency frequency of occurrence of occurrence). and F% = percentage frequency of occurrence).

Class Order Family n N% F F% Arachnida Araneae 10 2.34 7 25 Chilopoda 14 3.27 6 21.43 Diplopoda 3 0.7 3 10.71 Gastropoda 2 0.47 1 3.57 Stylommatophora 1 0.23 1 3.57 Polychaeta 46 10.75 14 50 Insecta Blattodea 1 0.23 1 3.57 Coleoptera 10 2.34 3 10.71 Carabidae 20 4.67 11 39.29 Scarabaeidae 9 2.1 3 10.71 Chrysomelidae 3 0.7 2 7.14 Curcullionidae 2 0.46 2 7.14 Curcujidae 1 0.23 1 3.57 Coccinellidae 3 0.7 2 7.14 Phalacridae 19 4.44 3 10.71 Dermaptera 4 0.93 3 10.71 Forfinculidae 5 1.17 2 7.14 Diptera 6 1.4 2 7.14 Stratiomyidae 49 11.44 5 17.86 Hemiptera Coreidae 1 0.23 1 3.57 Homoptera Acanaloniidae 1 0.23 1 3.57 Hymenoptera Apidae 1 0.23 1 3.57 Formicidae 165 38.55 23 82.14 Chrysididae 2 0.46 1 3.57 Evaniidae 1 0.23 1 3.57 Isoptera 2 0.46 1 3.57 Termitidae 20 4.67 3 10.71 Orthoptera Acrididae 5 1.17 5 17.86 Gryllidae 17 3.97 10 35.71 Gryllotalpidae 1 0.23 1 3.57 Pygomophidae 4 0.93 3 10.71

of consumed prey items (r ≤ 0.37, p ≥ 0.12- Fig. 3) Discussion and SVL and numerical abundance of consumed prey Most amphibians are generalist and opportunistic items for both males (n = 29 developed urban area, 10 invertebrate feeders (Santana et al., 2019), but certain farmland) and females (n = 16 developed urban area, species have become specialised on certain prey types 19 farmland). The only exception was that the SVL of (e.g., Smoky Jungle Frog, Leptodactylus pentadactylus; males from the urban area correlated negatively with the Do Couto et al., 2018). Our data suggest that S. regularis abundance of consumed prey items (Fig. 3). has a wide taxonomic range of their diet composition, supporting the findings from other studies on toad diets, such as Cane Toads, Rhinella marina (Pamintuan and Starr, 2016), Common Toads, Bufo bufo (Crnobrnja- 1172 Benjamin Yeboah Ofori et al.

Table 2. Taxonomic composition of prey items (n = 507) found in stomachs of Common African Toads, Sclerophrys regularis, from the developedTable 2. Taxonomic urban at thecomposition University of preyof Ghana’s items (n Legon = 507) Campusfound in stomachs(n = Number of Common of items, African N% Toads,= Numerical percentage, F = frequency Sclerophrysof occurrence regularis and F%, from = percentage the developed frequency urban at ofthe occurrence). University of Ghana’s Legon Campus (n = Number of items, N% = Numerical percentage, F = frequency of occurrence and F% = percentage frequency of occurrence).

Class Order Family n N% F F% Arachnida Araneae 6 1.18 4 8.89

Scorpiones 1 0.2 1 2.22 Chilopoda 2 0.39 2 4.44 Diplopoda 5 0.99 5 11.1 Gastropoda 1 0.2 1 2.22 Polychaeta 27 5.33 8 17.8 Insecta Blattodea Blattidae 2 0.39 2 4.44 Coleoptera 1 0.2 1 2.22 Carabidae 24 4.73 13 28.9 Scarabaeidae 17 3.35 6 13.3 Chrysomelidae 4 0.79 3 6.67 Curcujidae 1 0.2 1 2.22 Phalacridae 4 0.79 1 2.22 Dermaptera 1 0.2 1 2.22 Diptera 1 0.2 1 2.22 Stratiomyidae 1 0.2 1 2.22 Drossophilidae 2 0.39 1 2.22 Anthomyiidae 3 0.59 1 2.22 Hemiptera Cydnidae 4 0.79 2 4.44 Reduvidae 1 0.2 1 2.22 Hymenoptera Formicidae 375 74 41 91.1 Isoptera Termitidae 14 2.76 6 13.3 Kalotermitidae 1 0.2 1 2.22 Lepidoptera 1 0.2 1 2.22 Odonata Libellulidae 1 0.2 1 2.22 Orthoptera Gryllidae 4 0.79 4 8.89 Acrididae 2 0.39 2 4.44 Pyrogomorphidae 1 0.2 1 2.22

Isailović et al., 2012), and the congeneric species, of prey items (Crnobrnja-Isailović et al., 2012). Guttural Toads, Sclerophrys gutturalis (Baxter-Gilbert The most consumed prey items where from the taxa et al., 2021). Our findings also showed sex-specific Hymenoptera (Formicidae) and Coleoptera; similar to differences, with female toads consuming a wider what has been seen in other toad species (e.g., B. bufo; dietary niche breadth; which could be due to their Crnobrnja-Isailović et al., 2012). Given their strong increased energy requirements, particularly during the visual response to prey, associated with a sit-and-wait breeding season when they have higher metabolic rates foraging strategy, most toads are often believed to to support reproductive functions (Quiroga et al., 2015). consume whatever prey species are readily available Also, fecundity and egg size in amphibians depend on and widely abundant within a landscape (Moser et al., the nutritional quality of food (Van Ngo and Ngo, 2014). 2017). Therefore, the high frequency of occurrence and As such, females may meet their high nutritional quality numerical abundance of Hymenoptera (Formicidae) and energetic demands by consuming a broader diversity and Coleoptera in the diet of the toads would suggest Diet composition of the Common African Toad in a human-modified landscape 1173

Table 3. Differences between males and females Common African Toads, Sclerophrys regularis, in terms of the frequency of occurrence and numerical abundance of consumed prey items.

Order Site Frequency of occurrence Numerical Abundance Male Female χ2, p-value Male Female χ2, p-value Arachnida Developed area 12 6 2.00; 0.16 6 1 3.57; 0.06 Farmland 20 25 0.56; 0.46 2 8 3.60; 0.06 Blattodea Developed area 3 6 1.00; 0.32 1 1 0.00, 1.00 Farmland 0 5 - 0 1 - Chilopoda Developed area 6 0 - 2 0 - Farmland 10 25 6.43; 0.01 1 13 10.29; 0.001 Coleoptera Developed area 36 60 6.00; 0.01 19 32 3.314; 0.07 Farmland 80 60 2.86; 0.09 16 53 19.84; < 0.0001 Dermaptera Developed area 0 6 - 0 1 - Farmland 20 15 0.71; 0.40 4 5 0.11; 0.74 Diplopoda Developed area 6 18 6.00; 0.01 2 3 0.20; 0.66 Farmland 10 10 0.00; 1.00 1 2 0.33; 0.56 Diptera Developed area 6 12 2.00; 0.16 4 3 0.14; 0.71 Farmland 20 30 2.00; 0.16 5 49 35.85; <0.001 Gastropoda Developed area 3 0 - 1 0 - Farmland 0 5 - 0 3 - Hemiptera Developed area 6 6 0.00; 1.00 3 2 0.20; 0.66 Farmland 0 5 - 0 1 - Homoptera Developed area 0 0 - 0 0 - Farmland 0 5 - 0 1 - Hymenoptera Developed area 78 90 0.86; 0.36 292 83 116.48; < 0.0001 Farmland 100 95 0.13; 0.72 43 126 40.76; < 0.0001 Isoptera Developed area 15 12 0.33; 0.56 7 8 0.07; 0.80 Farmland 0 20 - 0 22 - Lepidoptera Developed area 3 0 - 1 0 - Farmland 0 0 - 0 0 - Odonata Developed area 3 0 - 1 0 - Farmland 0 0 - 0 0 - Orthoptera Developed area 12 18 1.20; 0.27 4 3 0.14; 0.71 Farmland 50 68 2.75; 0.10 7 19 5.54; 0.02 Polychaeta Developed area 18 12 1.20; 0.27 20 7 6.26; 0.01 Farmland 60 40 4.00; 0.05 16 30 4.26; 0.04

that these prey categories are the most abundant and gracilis (Graceful Dwarf Frog), suggesting dietary accessible prey within our study area. This assertion is niche conservatism in anurans. The high frequency of indeed supported by a recent survey from our study area occurrence and numerical abundance of Hymenoptera which found Hymenoptera (Formicidae) and Coleoptera (Formicidae) in the diet of the toads may also be due (Carabidae) to be the most abundant insects (Frimpong, to the social behaviour of these prey items (Moser et 2020). This finding supports the claim of Quiroga et al., 2017). Since these prey items are highly available in al. (2009) that Formicidae and Coleopterans are the the environment and are relatively easy to capture and dominant prey items in many toad species. Moser et process, their consumption is energetically rewarding for al. (2017) also found Formicidae and Coleopterans the toads (Van Ngo and Ngo, 2014). The high proportion to be the most important prey items in the diet of the of Formicidae in the diet of S. regularis could also be frogs Physalaemus lisei (Braun’s Dwarf Frog) and P. as a result of the fact that the species compensates for 1174 Benjamin Yeboah Ofori et al.

Figure 3. Correlation between SVL, diversity and abundance of consumed prey items by male and female common African toads from the developed area and farmland.

the small size of the prey by consuming large quantities abundance and diversity (i.e., SVL) and those which (Novitsky, 2003). do not (i.e., sex) may be due to the high degree of The body size (SVL) of S. regularis correlated variability in our data. Furthermore, the evident overlap positively with prey diversity and abundance, which in diet composition between females and males may suggests that larger individual toads consumed a higher be attributed to the use of the same microhabitat for variety and quantity of prey items – albeit this was foraging and intersexual competition for food resources not statistically significant. This generally follows the (Crnobrnja-Isailović et al., 2012). findings of Almeida et al. (2019) and Le et al. (2020) Overall, our findings show that these toads capitalise who attributed this to the relatively larger stomach on a wide range of prey items, suggesting that S. capacity that could accommodate large quantities of regularis is an opportunistic generalist predator. This prey items compared to smaller individuals. Also, larger feeding habit may be advantageous in dynamic habitats individuals tend to be more active and thus encounter and with constantly changing food availability. Our findings consume more diverse prey categories (see Mageski et highlights some of basic aspects of the ecology of al., 2018). These findings are of interest since we know common African toads and can be used to inform the that S. regularis is a sexually dimorphic species (Rödel, conservation and management of the species in their 2000) and body size was correlated with differences natural environment as well as in urban and other in prey diversity and abundance, however we did not human-dominated landscapes. detect a significant difference between females and males. The high level of dietary niche overlap (75% in Acknowledgements. The authors wish to thank Eudosia Obeng, farmland and 80% in the developed urban area) observed Charles Achina, Faustina Adu-Boahene, Patience Darko, and between females and males and the concordance in the Caleb Frimpong for their assistance in the field. distribution of various prey categories between females and males suggested the absence of sex-biased diet References niche partitioning. The discordance between what we Akinsanya, B., Isibor, P.O., Onadeko, B., Tinuade, A.A. (2020): observed regarding factors that are associated with prey Impacts of trace metals on African common toad, Amietophrynus Diet composition of the Common African Toad in a human-modified landscape 1175

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Accepted by Werner Conradie