Ethology Ecology & Evolution

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From diurnal to nocturnal activity: a case study of night-light niche expansion in Agama agama lizards

Nioking Amadi, Luca Luiselli, Robert Belema, Grace Awala Nyiwale, Chimela Wala, Nwaiwu Urubia & Roger Meek

To cite this article: Nioking Amadi, Luca Luiselli, Robert Belema, Grace Awala Nyiwale, Chimela Wala, Nwaiwu Urubia & Roger Meek (2021): From diurnal to nocturnal activity: a case study of night-light niche expansion in Agama￿agama lizards, Ethology Ecology & Evolution, DOI: 10.1080/03949370.2021.1883120 To link to this article: https://doi.org/10.1080/03949370.2021.1883120

Published online: 23 Feb 2021.

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From diurnal to nocturnal activity: a case study of night-light niche expansion in Agama agama lizards

1 1,2,3,* 1 1 NIOKING AMADI , LUCA LUISELLI , ROBERT BELEMA , GRACE AWALA NYIWALE , 1 1 4,† CHIMELA WALA , NWAIWU URUBIA and ROGER MEEK 1Department of Animal and Environmental Biology, Rivers State University of Science and Technology, Wildlife and Biodiversity Conservation Unit, Port Harcourt, Nigeria 2Institute for Development, Ecology, Conservation and Cooperation, Rome, Italy 3Département de Zoologie et Biologie Animale, Faculté des Sciences, Université de Lomé, Lomé, Togo 47 Rue George Clemenceau, Chasnais, France

Received 22 May 2020, accepted 1 December 2020

Most species of lizard are either diurnal or nocturnal, and it is extremely rare to find species that operate both diurnally and nocturnally, or that may shift from diurnality to partial nocturnality when conditions allow. However, niche expansion from diurnal to nocturnal habits (often referred to as the night-light niche) has rarely been reported in lizards (mainly in Anoles), and mostly through anecdotal reports. In West Africa, the rainbow lizard Agama agama is a conspicuous species across the region but also lives in suburban areas of towns and villages. It is a diurnal sun-basker operating at relatively high body temperatures of 36 °C and higher. In this paper, we describe a night-light niche expansion, i.e. nocturnal foraging and thermoregulation, in a small number of A. agama populations living in suburban areas. These lizards utilised radiant heat from incandes­ cent light bulbs situated on the walls of buildings to mostly achieve target body tempera­ tures and forage for and fed on five different groups of invertebrates. Foraging lizards had significantly higher body temperatures than inactive lizards. However, variance in body temperature was significantly greater in foraging lizards than in inactive lizards probably due to the necessity to shuttle between the incandescent night lights and cooler foraging areas during activity, a known cost of thermoregulation. Regression analysis of body temperatures against time of night in foraging lizards supported the notion that the lizards were maintaining body temperatures by actively thermoregulating whilst in inactive non-basking resting lizards during the same time period body temperatures declined. Although our results indicate a potential thermoregulatory benefit from using the night-light shift, we cannot be certain that this benefit is the direct cause of the shift, rather than an additional advantage when foraging.

KEY WORDS: Agamidae, niche shift, foraging ecology, thermal ecology.

*Corresponding author: Luca Luiselli, Institute for Development Ecology, Conservation and Cooperation, Via G. Tomasi di Lampedusa 33, 00144 Roma, Italy (E-mail: [email protected]). †Present affiliation for Roger Meek: Institute for Development, Ecology, Conservation and Cooperation, Rome, Italy.

© 2021 Dipartimento di Biologia, Università di Firenze, Italia 2 N. Amadi et al.

INTRODUCTION

Studies on diel activity patterns of lizards are central to understanding the evolution of behaviour, ecology and the mechanisms of coexistence with potential ectothermic vertebrate competitors (e.g., Pianka & Vitt 2006). In general, most species are either diurnal or nocturnal, with diel activity being one of the key niche partition­ ing elements (e.g., Pianka & Vitt 2006). It is therefore extremely rare to find species of lizard that operate both diurnally and nocturnally, or that may shift from diurnality to partial nocturnality when conditions allow (Russ et al. 2015; Gaynor et al. 2018). However, niche expansion from diurnal to nocturnal habits (often referred to as the night-light niche) has been observed in other reptiles, particularly species of Anolis lizards. For reptiles, there are both costs and benefits for a night-light niche shift. The theoretical advantages may be twofold, the first being thermal, since if appropriate body temperatures can be maintained for a longer foraging activity and feeding can be extended. A second is the physiological benefits, since nocturnal foraging may enable a lizard the opportunity to prey on abundant invertebrate clusters around the light bulbs which in turn may enhance growth and reproductive capacity through increased food uptake. However, there are potential costs including the risk of predation from nocturnal predators and increased competition with other species using the same light bulb resource (Perry & Fisher 2006; Perry et al. 2008). At present most observations on reptiles employing the night-light niche are anecdotal with systematic observations including a detailed examination of the theoretical costs and benefits currently lack­ ing. Examples of night-light niche expansions have also been observed in other animal groups, for instance in spiders (Frank 2009). The rainbow lizard (Agama agama) is one of the most cosmopolitan reptiles in Africa (Leache et al. 2009, 2017; Akani et al. 2013) being abundant in villages and towns where they live in small groups (Abulude et al. 2007; Mediannikov et al. 2012). Similar to geckos (Amadi et al. 2020a, 2020b), they are often active on walls and the ceilings of buildings or reside in small gardens, from where they feed on a high variety of arthropods (Abulude et al. 2007; Akani et al. 2013). Their adaptability has enabled introduced populations to succeed in semi-tropical conditions of Florida and Cuba (Enge et al. 2004; Borroto-Páez et al. 2015) indicating a high degree of ecological flexibility. The available scientific literature describes A. agama as a strictly diurnal active foraging heliotherm, that thermoregulates by basking in sunlit areas to raise body temperature and retreating to shaded areas to cool (Chapman & Chapman 1964; Cloudsley-Thompson 1981; Billawer & Heideman 1996; Anibaldi et al. 1998), but occasional sightings of nocturnal activity have been reported (Pauwels et al. 2004). In the present paper, we report the first quantitative study of nocturnal foraging and nocturnal thermal ecology of A. agama at localities of southern Nigeria (West Africa). We have evaluated these data in light of night-light niche theory. It proposes that that diurnal reptiles that are capable of using artificial light at night may be more successful when they are invasive species, thus A. agama may be an ideal candidate for adapting to a night-light niche shift. The capacity to successfully colonise new areas outside of Africa (e.g. Florida and Cuba) and to exploit highly altered biotopes support the notion of behavioural plasticity in this species (Chapman & Chapman 1964; Cloudsley-Thompson 1981). In this paper, we attempt to answer to the key question of what are the ecological correlates of the niche expansion/diel rhythm shift in foraging activity (from diurnal to nocturnal) among certain A. agama individuals, night-light niche expansion in Agama agama lizards 3 and we predict that fluctuating body temperatures in foraging lizards should exceed the fluctuations of body temperatures in inactive lizards.

MATERIALS AND METHODS

The study was conducted in three suburbs of Rivers State, Nigeria: Rumuagholu (Latitude 04°53.0729ʹN, Longitude 006°58.1186ʹE), Rumueme (Latitude 04°49.0279ʹN, Longitude 006° 58.6736ʹE) in Obio/Akpor Local Government Area, and Ogoloma (Latitude 4°73ʹ38.76N, Longitude 7°08ʹ11.03E) in Okrika Local Government Area of the State. The area is characterized by a forest-plantation mosaic, with numerous small villages and a few large urban centres, with Port Harcourt being the largest city in the state (Amadi et al. 2020b). The climate is tropical, with an extended wet season from March to September and a dry season from October to February. Ambient temperatures were almost constant throughout the year, ranging 27–32°C daily. The study was conducted only at night, from 8.30 pm to 3 am of each sampling night. A total of 56 days were spent searching for foraging lizards in the field (28 days by wet season and 28 days by dry season). Our observations on behaviour started in November 2019 through April 2020 when we searched around buildings with externally placed security (incandescent) light bulbs (n = 76) and also in the dark (n = 23). These were incandescent bulbs that give off a good level of heat. All sites were visited with the same frequencies, and both during the wet and dry season. With the aid of flashlights from four Tecno Camon 11 mobile phones (e.g. Amadi et al. 2020b), we carefully searched around buildings without externally positioned security lights for eventually active lizards. During these surveys, we encountered several lizards actively feeding on insects and to avoid pseudo-replication, each building was surveyed only once, so no multiple observations of the same lizards were made. When a lizard was seen attempting to secure prey, it was monitored for at least 10 min and prey types recorded. Actively foraging lizards were considered as “foraging” (FOR). The other two individuals that were observed thermoregulating and simply moving (but not foraging) were not considered as FOR, and were pooled with sleeping individuals as “non-foraging” (NONFOR), also because of their similar body temperatures with NONFORs. We registered temperatures of lizard’s body and the substrate with an infrared thermometer, 30 cm away from the lizard. More specifically, with a Benetech Lasergrip GM320 laser electronic 131 thermometer (0.1°C resolution and accuracy of ± 0.2 °C), the substratum temperature close to the light bulbs (Tbulb) where foraging lizards were seen was recorded along with body temperature (Tb) of the FOR individuals. We also recorded the substratum temperature of the spots where NONFOR lizards were observed (hereby Tsubstratum). Practically speaking, Tbulb is the equivalent of Tsubstratum but for FOR lizards. The temperature of each lizard and substratum were measured at the same distance (about 30 cm) as, usually, the measurement in this type of thermometer varies with distance. We always measured Tsubstratum at the immediate locality where the lizard was sitting. NONFOR lizards were typically observed on buildings without lights, walls, and on garden trees inside private properties. The activities displayed by the lizards around the light bulbs, apart from foraging, were also documented although not specifically used in the present paper. Regression analysis between time the day (measured as number of minutes after 8:30 pm), and Tb of (i) NONFOR and (ii) FOR lizards was made by Pearson’s moment product correlation coefficient. Differences among means of (i) Tbulb, (ii) Tsubstratum, (iii) Tb of FOR individuals, and (iv) Tb of NONFOR individuals were assessed by one-way ANOVA, followed by Tukey HSD post- hoc tests. Frequency differences between samples of foraging-at-night lizards by (wet versus dry) season were assessed by observed-versus-expected χ2 test. When multiple individuals were observed foraging under the same light, we considered that their sightings were not independent.

Thus, in these cases, they were considered as a single observation and the average lizard Tb was considered for the analysis. 4 N. Amadi et al.

Tests for the relationship between Tb and the probable heat source

A test of both inactive and foraging lizards body temperatures (Tb) and relationship to substrate (Ts) or light bulb temperature (Tbulb) was made using regression analysis. Substrate or light bulb temperatures were treated as the independent variables and body temperatures as the dependent variable. This gives, for example, in a test of Tb against Ts,

Tb ¼ b þ mεTs where m is the regression coefficient and b the y-intercept. If Tb is independent of Ts, m will have a value of 0 (e.g. Mann & Meek 2004). Non-moving lizards in an overnight retreat should have a body temperature that tracks the immediate Ts’s giving m a value of 1. In a second test, we assumed that a nocturnally active heliotherm (sun basker) in the absence of sunshine constrained to use incandescent night lights as a main heat source would shuttle between foraging areas and the night lights to maintain minimum optimum body temperatures. For a foraging lizard that is using a stationary heat source, it is predicted that Tb’s should be independent of time of night. The test for this is a regression of Tb against time of night determined as minutes after 2030 hr when observations began. This gives an equation of the form,

Tb ¼ b þ m � εTime where m is the regression coefficient, b is the y-intercept and ε is the white noise error. The latter incorporates measurement error and random variation (Gotelli & Ellison 2004). The test for thermoregulation is whether Tb is independent from time of night which requires that m should not depart significantly from a 0 regression coefficient. If the regression coefficient has a negative value significantly different from 0, then the lizards are not attempting to maintain Tb implying they are not actively thermoregulating. Comparisons with the theoretical coefficients in all regressions were made using the t-test described by Bailey (1995) with significance at α = 0.05.

Next we assumed that a foraging lizard attempting to maintain high Tb using a single limited heat source would have greater variation in Tb than resting lizards due to the requirements to shuttle between warm light bulbs and cooler foraging areas especially when heat availability in the foraging areas is lower than minimum preferred Tb. The prediction therefore is that fluctuating Tb’s in foraging lizards should exceed Tb fluctuation in inactive lizards. This was tested by comparing variation in Tb of foraging and inactive lizards using a two-tailed test F-test with a hypothesis H1: σ1 ≠ σ2. The Tb’s of both foraging and inactive lizards were normally distributed and hence comparison was by ANOVA. Preferred body temperature range of A. agama were obtained from James and Porter (1979) and we used minimum preffered Tbs as the key threshold that the lizards should attempt to maintain. We did not apply statistics to the food data because of the too small sample size. Statistical analyses were carried out by Statistica 6.0 version software and Minitab R17, with alpha set at 5%. In the text, the means are followed by ± one Standard Deviation except in the regression coefficients where it is Standard Error.

RESULTS

During our surveys, we made 336 observations of lizard individuals (106 males, 163 females, 67 juveniles), and in addition 18 FOR individuals (5.35%; 13 females, and 5 males; no juveniles) (Fig. 1). We also recorded a sample size of n = 133 Tsubstratum from NONFOR individuals. We never observed any lizards foraging by night in poorly lit, but only near incandescent bulbs. In six instances there were multiple individuals under the same heat source, in all cases, these “groups” consisted of only females. The frequencies of sightings of FOR lizards were slightly higher by wet season (63.6%) and did not differ significantly between seasons (χ2 = 0.45, df = 1, night-light niche expansion in Agama agama lizards 5

Fig. 1. — Photographic sequence of a A. agama foraging at night at the study area.

P = 0.503). The frequency of NONFOR lizards did not differ significantly between seasons (χ2 test with df = 1, P > 0.455). We observed at least some FOR Agama agama individuals from each of the three studied communities of Rivers State: nine inde­ pendent observations in Rumuagholu, five in Rumueme and four in Ogoloma; 100% of the FOR lizards were seen in buildings with light, whereas 71.3% (n = 318) of the NONFOR lizards occurred in dark buildings. We did not observe any NONFOR individual under the light bulbs. The lizards were observed feeding on flying ants (Hymenoptera Formicoidea, n = 11), Blattodea (n = 2), Isoptera (n = 3), moths (Lepidoptera, n = 6), and Coleoptera (n = 6) that were attracted to the incandescent bulbs. Interestingly, in a single case, after a heavy downpour on 2 April 2020 (in Rumuagholu), by 10:56 pm we observed two female Agama lizards feeding on multiple individuals of termites that were attracted to the light during their nuptial flight. We monitored the activities of these two individuals up until 11:00 am the following day, and observed that they neither left their sleeping microhabitat to feed nor bask in the normal way. Fifteen out of 18 individuals (78% of the observed lizards) were observed basking 2–4 cm close to the lamp holder, chasing and feeding on insects that entered the radius of the light (Fig. 1). Three other individuals entered the radius of the reflected light from the dark surroundings, and started to search for prey under the light. In one instance at Rumuagholu, a gecko (Hemidactylus brooki), situated 35 cm from an incandescent bulb, directly competed with a female A. agama for food, both simulta­ neously chasing insects. The univariate statistics of the temperatures recorded on the perching spots of NONFOR individuals (Tsubstratum) and under the incandescent bulbs (Tbulb) where FOR individuals were seen, as well as of the Tb for both NONFOR and FOR 6 N. Amadi et al.

Table 1.

Synopsis of the univariate statistics for the temperatures recorded on the perching spots (Tsubstratum) of non-foraging (NONFOR) individuals, and under the incandescent bulb (Tbulb) where foraging (FOR) individuals were seen, and body temperatures (Tb) of the two categories of lizard individuals (NONFOR and FOR). For the statistical details, see the text.

Tsubstratum Tb (NONFOR) Tbulb Tb (FOR)

N 336 336 18 18 Min 27.5 28.6 30 29.9 Max 38 36 49 39.1 Mean 32.23 31.94 43.17 36.18 Standard Error 0.44 0.25 1.16 0.48 Variance 6.82 2.30 24.15 4.16 Standard Deviation 2.61 1.52 4.91 2.04 Median 32.1 31.95 44 36.9

individuals, are given in Table 1. The means of these temperature variables differed significantly (ANOVA: F3,104 = 78.92, P < 0.0001), and Tukey HSD post-hoc tests revealed that: (i) Tsubstratum did not differ statistically from Tb in NONFOR (Tukey HSD post- hoc test: P = 0.983) but was significantly lower than either Tbulb or Tb(FOR) (Tukey HSD post-hoc test: in both cases P < 0.0001); (ii) The Tb’’s of FOR lizards (mean = 36.2 ± 2.04 °C) were higher than those of NONFOR lizards (mean = 31.9 ± 1.5 °C; ANOVA: F1,52 = 74.2, P < 0.0001) (Fig. 2) (Tukey HSD post-hoc test: P < 0.0001), and was significantly lower than Tbulb (Tukey HSD post-hoc test: P < 0.0001). The regressions of FOR lizards against Tbulb showed Tb increasing with increasing Tbulb (m = 0.35 ± 0.06) with t = 6.28, P = 0.0001 in a test of influence of Tbulb on Tb. The regression of Tb with Tsubstrate in NONFOR lizards gave a similar regression (m = 0.034 ± 0.09) with t = 3.6, P = 0.001 again showing a strong influence of Tsubstrate on Tb. These results indicate that the immediate thermal envir­ onments (heat from incandescent light bulbs in FOR lizards and wall temperatures in NONFOR lizards) had a strong influence on the Tb of both lizard groups. The regression coefficient of Tbs in resting lizards indicated a gradual decline in Tb as the night progressed and differed significantly from the 0 hypothetical coefficient required for evidence of active thermoregulation (m = 0.01 ± 0.001, t = 6.26, P = 0.0001). In contrast, foraging lizards maintained Tb as the night progressed with the regression coefficient not significantly different from 0 (m = 0.006 ± 0.004, t = 1.48, P = 0.16; Fig. 3). Fig. 3 shows the data along with lines derived from the corresponding equations. The Tb'’s of NONFOR individuals did not differ between lighted and dark build­ ings (t = 0.582, P = 0.563). Sixty-one percent (n = 11) of FOR lizard Tb’s were equal to or greater than the minimum preferred Tb, which in A. agama is ≈ 36 °C, the tempera­ ture that this species should normally begin basking to avoid further body temperature drop (James & Porter 1979). This compared to only 2.7% (n = 1, from in an illuminated building) of NONFOR lizards (z-test: z-score = 4.8, P < 0.05) (Fig. 2). Variance of Tb in night-light niche expansion in Agama agama lizards 7

Fig. 2. — Histograms of body temperatures in foraging Agama agama (FOR, upper) and inactive sleeping individuals (NONFOR). Broken lines indicate the minimum preferred body temperature in A. agama (≈ 36 °C derived from James & Porter 1979).

FOR lizards was significantly greater than in NONFOR lizards (ANOVA: F = 0.32, P = 0.005). The variation of Tb with time (Lagos standard time) in FOR lizards is presented in the Supplemental Data, Fig. S1.

DISCUSSION

The present study found that nocturnal foraging was present in suburban A. agama in Nigeria, and that both adult male and female lizards from three distinct 8 N. Amadi et al.

Fig. 3. — Graphs of foraging and resting lizard body temperatures plotted against time. Number of minutes are calculated from 2030 hr, the time when observations began. Lines running through the data points are derived from regressions that for resting lizards are; Tb= –0.006 ± 0.004 Time + 28.3 and foraging lizards, Tb = 0.006 ± 0.004 Time + 34.96. localities may exhibit this behaviour. The nocturnal shuttling between light bulbs and foraging areas mimics to some extent the diurnal behaviour of forest lizards where sunlit patches are sparsely distributed and lizards are constrained to shuttle between sunlit patches for heat and cooler areas of the forest to forage (e.g. Van Berkum et al. 1986). A shift in foraging times in a segment of the lizard population may serve to decrease the intensity of intra-specific competition indirectly favouring the night-light niche expansion in Agama agama lizards 9 establishment of high densities that otherwise would be limited by food availability. However, this behavioural modification may introduce direct inter-specific competi­ tion, with the sympatric and abundant thigmothermic gecko (Hemidactylus brooki) that normally forages at night (Amadi et al. 2020b). The main niche difference is that H. brooki feeds nocturnally with or without the presence of an artificial heat source (Amadi et al. 2020b), whilst A. agama feeds with natural daylight or only in the presence of artificial heat. Indeed, the thigmothermic H. brooki predominately utilised heat (33–38 °C) emanating from the walls (Avery 1982; Amadi et al. 2020b). However, our study cannot disentangle whether (i) lizards actively bask underneath light bulbs to reach optimal body temperatures, which allows them to forage (although they clearly attain higher body temperatures by doing so) or (ii) lizards are attracted to the high abundance of insects near these light bulbs and warm up due to foraging near them. The relationship between the two groups of lizards’ Tbs is actually due to different substrate temperatures; NONFOR lizard substrate temperatures were those taken on unlit areas, while on foraging lizards they were substrate temperatures next to lamps. What is clear, however, is that the two groups of lizards fitted the classical thermoregulatory paradigm predicting that variance of Tb in FOR lizards should be greater than in NONFOR lizards due to the requirement to shuttle between different heat regimes in the former. It was also supported by the decline in FOR lizard Tb as the night progressed compared to FOR lizards’ Tb levels that were maintained and even increased slightly (see Fig. 3). By basking and achieving higher Tb’s compared to inactive lizards, foragers actually gain in two ways; they increase feeding rates and the increased Tb’s should enable more efficient securing of prey due to Q10 effects. This is due to most biological reactions have Q10s of around 2–3; for example, a Q10 of 2 for muscular energy between 20 and 30 °C indicates an increase of twice the amount of energy available in the muscles over that particular increase in temperature range, therefore enhancing prey capture and flight from predators. This will also result in an increase in digestive efficiency increasing growth and reproductive effort. Interestingly, when multiple individuals were observed under an incandescent bulb, these were only-female aggregations. We never observed any only-female aggre­ gations in diurnally foraging A. agama that, instead, they do behave in typical terri­ torial groups (one male and several females; N. Amadi et al. unpublished data). Thus, the observed aggregation behaviour of nocturnally foraging females mirrors observa­ tions that gecko densities can be a lot higher beneath artificial light compared to more natural conditions (Lozano-Del Campo & García-Roa 2014). According to Lozano-Del Campo and García-Roa (2014), this unusual tolerance of the presence of other individuals in such a reduced but suitable place, during predatory behaviour including a spotlight, could be explained as an adaptive strategy to increase predation success. Although based on a relatively small sample size, the diet of nocturnally foraging lizards was qualitatively similar to that of diurnally active individuals that were studied in the same Port Harcourt area by Akani et al. (2013). Formicoidea, Coleoptera and Lepidoptera represented important prey sources in both lizard “categories”. The lizards did not vary significantly between seasons in terms of frequency of nocturnally active and foraging individuals. This result is not surprising given that the ambient temperatures were very constant at the study localities. Differently, in two species of Egyptian geckoes studied to date (Perry et al. 2008), night-light niche expansion was observed mainly during cold periods. Interestingly, rainfall patterns 10 N. Amadi et al. also did not appear to influence the frequency of nocturnally active and foraging individuals, despite rain being one of the main factors influencing the foraging ecology of tropical reptiles (e.g. Dendi et al. 2019). It is recognized that comparing the Tb of reptiles with the immediate surrounding temperatures may be controversial because Ts cannot be used to evaluate thermal offer as probably the lizard chose that spot because of its temperatures (see Dreisig 1984; Hertz et al. 1993). However, environmental temperatures nevertheless provide a degree of insight into heat exchange rates between a reptile and its environment (Peterson et al. 1993). Since temperatures and radiation levels are normally lower at night, reptiles are usually constrained to operate as thigmotherms and hence temperature differentials can be expected to be lower. The required levels of thermoregulatory effort and availability of heat sources to achieve preferred Tb’s must be the normal constraining element for nocturnal activity in A. agama since heat availability is more limited compared to daytime levels, indeed this assumption may explain the limited numbers of lizards that are nocturnally active. This might suggest that a typical heliothermic lizard would be unlikely to become a serious competitor species for nocturnally active gecko lizards (especially, given the relative body size differences, between juvenile agama and adult geckoes). In this regard, we also documented direct predation of A. agama on sympatric geckoes at our study areas (Fig. 4). However, the results presented here nevertheless demonstrate a high degree of plasticity in thermoregulation in A. agama. For example,

Fig. 4. — Direct predation of Agama agama on a sympatric gecko at the study area in southern Nigeria (photo E.A. Eniang). night-light niche expansion in Agama agama lizards 11 much higher radiation levels are available during daylight hours in Nigeria (Peterson et al. 1993), the climatic space where the preferred Tb range of A. agama has evolved. The requirement to shuttle between light bulbs and cooler areas of walls (just 10–20 cm outside the lighted area) may reduce foraging distance and enhance prey availability when insects are hovering around the bulbs (Peterson et al. 1993). Obviously the behavioural changes of A. agama from diurnal to nocturnal activ­ ity may also have negative effects of their survival, for instance an enhanced risk of predation. At the study area, snakes and cats are the two main predators of these lizards (Amadi et al. 2020a), and both these predators are more active during the night. Thus, it is very likely that an increase of predation risk would occur for nocturnally active A. agama. The suburban areas of towns and cities are frequently reported as the most rapidly changing environments, producing fragmented landscapes that are a prime cause of loss of biodiversity (e.g. Fischer 2000). They change the degree of predation risk (e.g. Evans 2004), reduce species abundance and alter the thermal environment (Zhou et al. 2011). This latter factor is of particular interest since few, if any, detailed studies have been carried out on this and how ectothermic reptiles respond to the thermal changes in suburban areas. In this paper, we have shown that not only has A. agama been able to adapt to the new conditions but some sections of the popula­ tions have harnessed available artificial heat sources to extend their thermal niche and forage nocturnally. The next phase of this study is to examine the wider thermal niche of A. agama outside urban environments using null models and to monitor daily body temperatures in these natural environments. Hopefully, this will provide additional insight into the extent of adaptability in both behaviour and thermal tolerances in this remarkable species.

DISCLOSURE STATEMENT

No potential conflict of interest was reported by the authors.

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