Resource density regulates the foraging investment in higher termite species

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1 Ecological Entomology (2018), 43, DOI: /een Resource density regulates the foraging investment in higher termite species CAMILLA S. ALMEIDA, 1,2 PAULO F. CRISTALDO, 2 OG DESOUZA, 3 LEANDRO BACCI, 4 DANIELA F. FLORENCIO, 5 NAYARA G. CRUZ, 1,2 ABRAÃO A. SANTOS, 4,6 ALISSON S. SANTANA, 4 ALEXANDRE P. OLIVEIRA, 4,6 ANA P. S. LIMA 4 and ANA P. A. ARAÚJO 2 1 Ecological Interactions Laboratory, Post Graduate Program in Ecology and Conservation, Federal University of Sergipe, São Cristóvão, Brazil, 2 Ecological Interactions Laboratory, Department of Ecology, Federal University of Sergipe, São Cristóvão, Brazil, 3 Termitology Laboratory, Department of Entomology, Federal University of Viçosa, Viçosa, Brazil, 4 Department of Agronomic Engineering, Federal University of Sergipe, São Cristóvão, Brazil, 5 Department of Agrotechnology and Social Sciences, Federal Rural University of the Semi-Arid, Natal, Brazil and 6 Department of Agronomic Engineering, Post Graduate Program in Agricultural and Biodiversity, Federal University of Sergipe, São Cristóvão, Brazil Abstract. 1. Resource density can regulate the area that animals use. At low resource density, there is a conflict in terms of balance between costs of foraging and benefits acquired. The foraging of the higher termite Nasutitermes aff. coxipoensis consists of searching throughout trails and a building galleries phase. 2. In this study, a manipulative field experiment was used to test the hypothesis that colonies of N. aff.coxipoensis forage towards a more profitable balance between the establishment of trails and gallery construction at low resource density. 3. The experiment was conducted in north-eastern Brazil. Seven experimental plots were established with a continuous increase in resource density (sugarcane baits). Entire colonies of N. aff.coxipoensis were transplanted from their original sites to the experimental plot, totalling 35 nests. The number, branches and total length of trails and galleries were quantified. 4. The results show that N.aff.coxipoensis optimises its foraging output, intensifying the establishment of trails at the cost of gallery construction when resource density is low. The number of trails, the number of trail branches and the total length of trails decreased with increasing resource density. Interestingly, at low resource density, the search effort was concentrated on forming longer and a greater number of trails, a small proportion of which were converted into galleries. The opposite relationship was observed at high resource density. 5. These results suggest an optimisation of search efforts during foraging depending on resource density, a mechanism that may help researchers to understand the use of space by higher termite species. Key words. Food searching, foraging area, Isoptera, Nasutitermes, resource density. Introduction Foraging behaviour can be influenced by intrinsic biological characteristics and individual capabilities, as well by internal Correspondence: Ana P. A. Araújo, Department of Ecology, Federal University of Sergipe, São Cristóvão, Sergipe, Brazil. anatermes@gmail.com and external environmental factors such as starvation and resource density, respectively (Bell, 1990). Balancing the costs and benefits of foraging (Pyke et al., 1977) can result in changes in the extent of home range, with consequences for ecological processes (see Börger et al., 2008). One hypothesis of home range regulation suggests that if animals accumulate enough resources to satisfy their minimum biological threshold, they will use the smallest area possible to provide the necessary 2018 The Royal Entomological Society 371

2 372 Camilla S. Almeida et al. energy for survival and reproduction ( area minimisation strategy ; Mitchell & Powell, 2004). Empirical evidence has supported this idea, indicating a negative relationship between foraging area and resource density (Ford, 1983), in both vertebrates [e.g. mammals (Saitoh, 1991; McLoughlin et al., 2000; Jorge & Peres, 2005; Mitchell & Powell, 2007), birds (Carpenter & MacMillen, 1976; Hixon et al., 1983; Powers & McKee, 1994)] and invertebrates (e.g. ants; Urbas et al., 2007). Starvation serves as a stimulus for animals to actively forage (Bell, 1990), and under low resource density, extensive foraging may promote conflict in terms of balancing costs and benefits. In this situation, it seems that animals cannot achieve optimal foraging unless they have the ability to minimise these costs. Foraging costs could be even more pronounced for so-called central place foragers, animals with foraging systems constrained around nests (e.g. almost all eusocial insects) (Kotler et al., 1999; Brown & Gordon, 2000). Unlike animals that feed at the resource location, central place foragers must return to the nest with food item(s). To handle this task, they have complex signalling mechanisms that are used to share information during foraging, such as warning of predation risk and recruitment to the food source (Beekman & Lew, 2008). In higher termite species (i.e. Termitidae), central place foraging strategy is traditionally known to include open-air foraging (above ground in exposed processional columns) or the construction of a network of subterranean tunnels that link the nest to food sources (Grace & Campora, 2005) (but see Almeida et al., 2016). In the latter case, termites excavate a matrix composed of main tunnels with secondary branches that can span hundreds of metres. These tunnel networks should confer some benefits to termites during foraging, such as protection against predators and adverse abiotic conditions (Buczkowski & Bennet, 2008). As the initial food search phase is extremely costly in terms of energy, excavating tunnels at random until food is discovered is probably not an optimal foraging strategy. Furthermore, tunnels are an ephemeral investment because they might be abandoned if food resource decreases or local foraging risk increases, adding extra constraints to already costly excavating processes (Campora & Grace, 2001). In addition, unlike other animals that can change their foraging locality under low food resource conditions, termite colonies are not able to move their colonies to other, more profitable sites (but see Thorne & Haverty, 2000). In resource-deprived sites, these costs can be unbearable because under the threat of starvation, food-searching stimuli are enhanced but the energy to search is limited (Bell, 1990). This elevated cost of food searching suggests that colonies should adjust their home use in response to resource density, using the smallest area possible to provide the required energy ( area minimisation strategy ; Mitchell & Powell, 2004), independently of the foraging strategy employed. Most studies of termite foraging behaviour have evaluated subterranean species in artificial laboratory systems (Hedlund & Henderson, 1999; Arab & Costa-Leonardo, 2005; Gallagher & Jones, 2005; Lee & Su, 2010; Araújo et al., 2011). To our knowledge, no direct experimental approaches have been used to evaluate termite search effort during foraging in response to resource density in natural environments. Nasutitermes aff. coxipoensis occurs in north-eastern Brazil, in sandbank areas with grasses interspersed by open dunes. Foraging by N. aff. coxipoensis comprised two sequential behaviours: the establishment of trails followed by the construction of galleries on the soil surface (Almeida et al., 2016). Foraging by N. aff.coxipoensis begins in the early evening with the establishment of trails on the soil surface the labour is carried out by members of both worker and soldier castes. The galleries were constructed after an initial exploration of the trails and were usually built on trails that were not directly connected to the nest, as previously showed by Almeida et al. (2016). This species builds epigeous nests frequently found in grasslands surrounded by open dunes (A.P.A. Araújo, pers. obs.). According to Mathews (1977), grasses and dead wood seem to be the main food sources of N. coxipoensis. In the north-east of Brazil, N. aff. coxipoensis was already observed feeding on dead steams of sugarcane (Miranda et al., 2004). Here, we assess whether an alternative strategy exists in which termites may reduce the costs of foraging while maintaining efficiency in food discovery. We observed foraging decisions made by N.aff.coxipoensis termite colonies after transplantation to sandbank sites with controlled densities of food resource. We showed that termites foraging effort is regulated by resource density and that these insects employ a strategy to maximise the search effort in resource-deprived sites by establishing more trails than galleries. Materials and methods Ethics statement and species identification Permits for termite collection were issued by ICMBio, IBAMA ( ). Nasutitermes aff. coxipoensis were individually identified and the voucher specimens (#UnB-10616, 10617, 10618, 10619, 10620, 10621) are deposited in the collection of the Termitology Laboratory at the University of Brasilia. Study area The experiment was conducted in March 2015 ( dry season ) at the Santa Isabel Biological Reserve ( S, W) in Pirambu, Sergipe, north-eastern Brazil. The landscape is dominated by native Brazilian Atlantic coast vegetation ( Restinga ), which consists of grasslands (grasses and sedges) and post-beach, sandbank, palm trees, wetlands and marshes. The climate in this region is characterised as megathermic humid and sub-humid, with annual precipitation between 1500 and 1800 mm and a mean annual temperature of 26 C. The climate in this region is tropical wet and dry (Aw) according to Köppen climate classification systems. Experimental procedure Foraging habits of N. aff.coxipoensis colonies were evaluated by manipulating food resource density (baits; see later) in homogenous open-dune areas (interspersed with native

3 Resource and termite foraging 373 (a) (b) (*) (*) transplanted nests transplanted nests (*) (c) (d) trail gallery gallery open-air foraging Fig. 1. Photographs of the field experiment to evaluate Nasutitermes aff. coxipoensis foraging. (a, b) Manipulation of food resource density was conducted in homogenous open-dune areas (interspersed with native Restinga areas) totally devoid of vegetation, and with no visible item that could represent a resource for termites (i.e. roots, wood, litter). (c, d) View of one N.aff.coxipoensis nest transplanted to the experimental plot and trails and galleries observed around the nest during the experiment. [Colour figure can be viewed at wileyonlinelibrary.com]. Restinga areas) totally devoid of vegetation, and without any visible item that could represent resources for termites (i.e. roots, wood, litter) (see Fig. 1). Seven plots (16 m 16 m) were established with different resource densities, forming 5 5 m quadrants, with a central quadrant surrounded by four peripheral quadrants separated by a distance of 0.5 m (Almeida et al., 2016). One N. aff. coxipoensis colony was transplanted to the centre of each quadrant (see later), for a total of five nests per plot. The minimum distance between plots was 3 m. Resource manipulation The number of food items available in time and space influences the rate of energy acquisition by foragers (Bell, 1990). Thus, a reduction in the resource density could promote higher foraging costs due to the increase in time and energy spent searching for food (Chase, 1998). Specifically for N. aff. coxipoensis that need to search for food and then build galleries, the costs to searching for scarce resources may even be greater. To these animals, food density, and consequently the chances of finding food, can be interpreted from the perspective of the colony position, which can be influenced by two factors simultaneously: (i) resource proximity relative to the nest; and (ii) resource quantity. The more distant and scarce a resource is in relation to the nest ( low density ), the greater the costs, and vice versa. Previous tests conducted by us have shown that the factors resource proximity related to the nest and resource quantity resulted in the same foraging pattern in N. aff.coxipoensis (see SM01). Thus, we combined these two factors and, in the present study, we used density (i.e. number of baits/area) as a surrogate for the relative difficulty of finding (in terms of energy) and using a food resource for termite colonies, where greater density of baits in the plot means lower energy costs for termite colonies and vice versa. The manipulation of resource densities was conducted by delimiting six concentric circumferences around the nests. The first circumference was positioned immediately on the nest side and the next ones were positioned 0.5 m apart each other. Resources (baits) were distributed in each circumference at eight points (e.g., the cardinal and side directions). Baits consisted of fresh sugarcane stems (15 cm length 2 cm radius). Within each plot, all quadrants contained identical resource distribution and quantity. The total amount of resources per quadrant (25 m 2 ) ranged from 0 to 48 baits (N = 840 baits), which represented a resource density gradient from 0 to 1.92 baits m 2 across plots. Baits were inspected daily and it was replaced when necessary. Any potential resource fragments that fell into the grid (e.g., small fragments of branches and leaves) were removed each morning. Nasutitermes aff. coxipoensis nest transplants Entire nests were removed between 06:00 and 11:30 hours and deposited on trays using shovels and picks. Immediately after removal, the nests were transplanted at a minimum distance of 50 m from the original location. Holes (30 cm deep)

4 374 Camilla S. Almeida et al. (a) (b) (c) (d) 0 bait m baits m baits m baits m 2 (e) (f) (g) Tr ails Galleries Resource bait N. aff coxipoensis nest 1.28 baits m baits m baits m 2 Fig. 2. Representative variation of Nasutitermes aff. coxipoensis foraging in nests with distinct resource density, after 10 days of nest implantation. (a g) Maps of trails and galleries of the one representative nest of each plot with distinct resource density ( baits m 2 ). [Colour figure can be viewed at wileyonlinelibrary.com]. were dug in the centre of each quadrant where nests were then inserted, and nest bases were covered with local soil. The initial volumes of transplanted nests were similar among plots [anodev, F 1,6 = 0.329, P = 0.591; ± 1.31 liters (mean ± SE)], which indicates that foraging capacities were similar among transplanted colonies. Preliminary tests indicated that transplantation did not affect colony survival (Almeida et al., 2016). Only undamaged nests and active colonies were used (N = 35). The activity of the colonies was measured according to DeSouza et al. (2016) (see experimental physical disturbance). Evaluation of search effort during termite foraging We evaluated colony search efforts during foraging by direct observation daily after 24 h of nest transplantations over 10 consecutive days. For each nest, we quantified: (i) the total number of trails and galleries; (ii) the number of branches from trails and galleries; (iii) the length (cm) of trails and galleries; and (iv) the gallery construction speed (cm day 1 ). We also estimated the rate of trails converted into galleries by dividing the gallery length by the trail length. Here we use galleries to refer to the structure constructed by termites above the soil surface, while trails refer to the traces made by termites during open-air foraging on the soil surface (Fig. 1d). Data analysis All analyses were carried out in r (R Development Core Team, 2015) using generalised linear mixed models (GLMMs) followed by residual analysis to check model assumption and model quality. The variations in the total number of trails and galleries, the total number of branches in trails and galleries, and the total length (cm) of trails and galleries (y-vars) were analysed as a function of resource density (x-var). Tests for each y variable were done separately using mixed linear regression analyses with Poisson error distribution corrected for overdispersion with quasi-poisson (i.e. number of trails and galleries, number of branches in trails and galleries) and Guassian distribution [i.e. length (cm) of trails and galleries]. For the gallery construction speed (cm day 1 ) and the rate of trails converted into galleries (gallery length/trail length) we used a negative binomial error distribution. Results After 10 days of nest transplantation it was possible to observe variations in the N. aff.coxipoensis foraging in nests with distinct resource density (see the most representative maps on Fig. 2). In general, there was a higher search effort in places with low resource density. On average, N. aff. coxipoensis colonies established a greater number of primary trails in places with low resource density (i.e baits m 2 ) (quasi-poisson GLMM, Wald s t-test, d.f. = 35, t = 4.731, P = 0.009; Fig. 3a) and the number of branches in trails reduced with resource density (quasi-poisson GLMM, Wald s t-test, d.f. = 35, t = 9.069, P = 0.003; Fig. 3b). The total length of trails significantly decreased with increasing resource density (negative binomial GLMM, z-test, d.f. = 35, z = 3.746, P = ; Fig. 3c). For building effort, in general, there is a greater effort on intermediate resource density. The total number of primary galleries was

5 Resource and termite foraging 375 (a) (b) (c) y = exp( x x 2 ) y = exp( x) (d) (e) (f) y = exp( x) y = x) No. of gallery branches No. of trail branches y = exp( x x 2 ) Resource density (baits m 2 ) Resource density (baits m 2 ) Resource density (baits m 2 ) Fig. 3. Trail formation and gallery behaviour of Nasutitermes aff. coxipoensis in plots with different resource densities. (a) Effects of resource density (baits m 2 ) on total number of trails; (b) total number of primary branches of trails; (c) total length of trails; (d) total number of galleries; (e) total number of primary branches of galleries; (f) the total length of galleries.

6 376 Camilla S. Almeida et al. Fig. 4. Variation of gallery length (cm) with time after nest transplantation in plots with different resource densities ( baits m 2 ). Each point represents the mean activity of the five nests on each day post-transplantation. [Colour figure can be viewed at wileyonlinelibrary.com]. not significant affected by resource density (quasi-poisson GLMM, Wald s t-test, d.f. = 35, t = 1.597, P = 0.171; Fig. 3d). However, the number of gallery branches peaked at a resource of 0.64 baits m 2 (quasi-poisson GLMM, Wald s t-test, d.f. = 35, t = 3.047, P = 0.028; Fig. 3e). The total length of galleries peaked at a resource of 0.64 baits m 2 (negative binomial GLMM, z-test, d.f. = 35, z = 3.52, P = ; Fig. 3f). Figure 4 shows the variation of gallery length (cm)/nest with time after nest implantation. The gallery construction speed (cm day 1 ) also peaked at a resource of 0.64 baits m 2 (negative binomial GLMM, z-test, d.f. = 35, z = 3.543, P = 0.003). The results show that termites construct proportionally longer galleries than trails on sites with higher resource density (i.e baits m 2 ) (negative binomial GLMM, z-test, d.f. = 35, z = 2.924, P = 0.003; Fig. 5). The total variation in trails and galleries of N. aff. coxipoensis with time after nest transplantation for plots with different bait density is shown in Fig. SM02. Discussion Our results indicate that the size of the trails/galleries foraging in N. aff. coxipoensis colonies is regulated by resource density The increase in foraging efforts in sites with low resource density (i.e baits m 2 ) occurs through the establishment of more and longer trails (Fig. 3a c). However, in colonies with low resource density (0 and 0.32 baits m 2 ), the proportion of established trails converted into galleries was less than in those with high resource density (1.92 baits m 2 ) (Fig. 5). These results indicate that termite colonies with low resource density increase their search efforts during foraging, as expected when the chance of resource encounter is low. However, high foraging effort seems to be minimised by the initial establishment of trails (lower energy costs) which are then converted into galleries more frequently in places with more profitable resources (e.g. with intermediate to high resource density) (Fig. 5). Fig. 5. Proportion of gallery length in relation to trail length in plots with different resource densities. The conversion of trails to tunnels increases with higher resource density. Each point represents the mean activity of the five nests over 10 days of post-transplantation in quadrants with different resource densities. The total number of gallery branches was highest in area with 0.64 baits m 2 of resource (Fig. 3e). Gallery branches have been reported to be responsible for increased exploitation of the foraging area by connecting distinct food sources that are used simultaneously (see Arab & Costa-Leonardo, 2005). Gallery construction speed also peaked at intermediate resource density ( baits m 2 ). In this situation, when resources are present but not in high abundance (i.e. intermediate density), termite hunger can serve as a stimulus to increase the gallery construction speed. In fact, starvation has been considered as a stimulus to ants to follow a pheromone trail which leads to the discovery of food, to start the exploration of new food sources (von Thienen & Metzler, 2016) and to increase recruits (Mailleux et al., 2010). However, when resources are limited or absent (low stimulus), termite colonies converted trails into galleries at a slow rate. This rate is due to low habitat profitability, resulting in a lower rate of construction. At higher resource density, the greater proximity of resources to the nest eliminates the necessity to increase the search effort. These results indicate that N.aff.coxipoensis colonies optimise food-searching effort by using an area minimisation strategy (as proposed by Mitchell & Powell, 2004). Taken together, our results and the results shown by Almeida et al. (2016) suggest that N. aff. coxipoensis colonies perform directional foraging (from the nest to resource baits), and thus optimise energy and time expenditure. The foraging strategy of N. aff. coxipoensis colonies (e.g. foraging in trails and gallery) seems to promote optimisation through reduction of the conversion rate of established trails into galleries at unprofitable sites (Figs 2 and 5), as initially suggested by Almeida et al. (2016). This strategy can promote a more efficient cost/benefit balance compared with species that

7 Resource and termite foraging 377 only forage underground (i.e. via tunnels; subterranean termite species). Irrespective of the mechanisms involved in the foraging of different termite groups, the strategy presented here to N. aff. coxipoensis is a novel one and could be useful in discussions about the evolution of the foraging behaviour of termite species. The foraging strategy shown here is part of a behavioural repertory adjusted along the diversification of the Isoptera clade, following the complete separation between nest and food resource (see Almeida et al., 2016). Studies among different hierarchical levels of biological organisation (e.g. plant stolons, fungi system of hyphae, foraging in trails) have found similar results according to resource abundance (Rayner & Franks, 1987), regardless of their origins, size and functionality (López et al., 1994a). Studies of stoloniferous or rhizomatous herbs and trunk trail systems in ants have revealed different resource capture strategies: a decrease in the length of plant internodes and greater trail branching in resource-rich sites ( phalanx strategy ), and an opposite strategy in resource-poor sites ( guerrilla strategy ) (López et al., 1993, 1994a,b). Our results also show numerous and longer trails among sites with low resource density, but less branching when resources increase. These results could be related to the main function of the trails for termites, which is to search for food, whereas for ants it is to retrieve food to the nests. However, it is important to highlight that foraging and termite exploitation of the environment are part of a dynamic process that can be modified by other environmental factors [e.g. temperature (Arab & Costa-Leonardo, 2005; Cornelius & Osbrink, 2011), water (Hu et al., 2012), soil (Evans, 2003; Lima & Costa-Leonardo, 2012), obstacles (Pitts-Singer & Forschler, 2000)] and intrinsic colony needs [i.e. colony growth (Traniello & Leuthold, 2000), colony size (Su et al., 2017)] as well as by resource offer. The inverse relationship between resource density and foraging area has also been shown in ants (Brown & Gordon, 2000; Leal & Oliveira, 2000; Urbas et al., 2007) and other eusocial insects (see Richter, 2000; Westphal et al., 2006). Leaf-cutting ants reduced trail length and foraging area on the edges of forests, which have an increased proportion of more palatable resources (i.e. pioneer plants); foraging areas were increased in the forest interior where resource suitability was low (i.e. greater abundance of defensive plants) (Urbas et al., 2007). Similarly, ants prefer to use food items closer to the nest when resources are abundant (Brown & Gordon, 2000). However, to the best of our knowledge, the current study is the first to show a reduction of foraging area with increased resource density for N. aff. coxipoensis colonies in field conditions. The present study shows that resource density directly influences the home range used by N. aff.coxipoensis colonies. These results suggest that this species evaluates the environment and is able to respond to local conditions by adjusting cost benefit relationships during foraging processes. 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