Journal of Science: Vol. 13 | Article 71 Khelifa et al.

Niche partitioning in three sympatric congeneric species of , chrysostigma, O. coerulescens anceps, and O. nitidinerve: The importance of microhabitat

Rassim Khelifa¹*, Rabah Zebsa¹, Abdelkrim Moussaoui², Amin Kahalerras¹, Soufyane Ben- souilah¹, Hayat Mahdjoub¹

¹Département d’écologie et du génie de l’environnement, Université 08 Mai 1945, Guelma 24000, Algérie ²Laboratory of Electrical Engineering, Guelma (LGEG), Université 08 Mai 1945, Guelma

Abstract heterogeneity has been shown to promote co-existence of closely related species. Based on this concept, a field study was conducted on the niche partitioning of three territorial conge- neric species of skimmers (Anisoptera: ) in Northeast during the breeding season of 2011. According to their size, there is a descending hierarchy between Orthetrum ni- tidinerve Sélys, O. chrysostigma (Burmeister), and O. coerulescens anceps (Schneider). After being marked and surveyed, the two latter species had the same breeding behavior sequence. Knowing that they had almost the same size, such species could not co-occur in the same habitat according to the competitive exclusion principle. The spatial distribution of the three species was investigated at two different microhabitats, and it was found that these two species were actually isolated at this scale. O. chrysostigma and O. nitidinerve preferred open areas, while O. c. anceps occurred in highly vegetated waters. This study highlights the role of microhabitat in community structure as an important niche axis that maintains closely related species in the same habitat.

Keywords: breeding behavior, habitat preferences, niche overlap Correspondence: [email protected], *Corresponding author Received: 12 January 2012 Accepted: 27 March 2013 Copyright: This is an open access paper. We use the Creative Commons Attribution 3.0 license that permits unrestricted use, provided that the paper is properly attributed. ISSN: 1536-2442 | Vol. 13, Number 71

Cite this paper as: Khelifa R, Zebsa R, Moussaoui A, Kahalerras A, Bensouilah S, Mahdjoub H. 2013. Niche partitioning in three sympatric conge- neric species of dragonfly, Orthetrum chrysostigma, O. coerulescens anceps, and O. nitidinerve: The importance of microhabitat. Journal of Insect Science 13:71. Available online: http://www.insectscience.org/13.71 Journal of Insect Science | http://www.insectscience.org 1

Journal of Insect Science: Vol. 13 | Article 71 Khelifa et al. lar exclusions between morphologically simi- Introduction lar species. Brown and Wilson (1956) stated that such species would adopt character dis- Processes that determine species’ coexistence placement (morphological differences and exclusion are central topics in community between closely related species coexisting in ecology. According to Hutchinson (1957), an the same area) as a solution when they live in ecological niche is an n-dimensional hyper- sympatry. Moreover, predation and competi- space where each axis (dimension) represents tion for resources have also been shown to a resource or an environmental condition. A determine species coexistence by specifically common assumption is that sympatric species excluding groups of species (McPeek 1989, with a similar phenotype tend to reduce con- 1990). For example, within the genus of Enal- flict by occupying different niches (Colwell lagma, some species were found resident in and Fuentes 1975). The more the overlap in fishless while others were only found in species’ niche, the stronger the competitive lakes containing fish in many North American interactions between them (Hardin 1960). Of lakes (Johnson and Crowley 1980; Crowley course, given the many aspects of a niche, and Johnson 1982; McPeek 1989, 1990). measuring a species’ entire niche is impossi- ble. However, Schoener (1974) proposed Adult odonates, which are usually territorial microhabitat, diet, and temporal activity as the during the breeding season, are a good biolog- three most important niche axes, and subse- ical model for inter- and intraspecific quently a large range of empirical data competition studies (Moore 1964). Usually, regarding these components in several mature males defend a specific territory groups has become available, for example in against intruders and thus attempt to dominate mammals (Doniol-Valcroze 2008), birds access to females (Corbet 1999). Given the (Salewski et al. 2002; Parra et al. 2004), rep- limited availability of suitable breeding habi- tiles (Metzger et al., 2009), amphibians tats and females, territories can be considered (Kuzmin 1990; Behangana and Luiselli 2008), as a limited resource for which territorial and (Heinrich 1976; Coderre 1987; males regularly compete during this period. Crowley and Johnson 1982; Gilbert et al. Usually, the intensity of intra- and interspecif- 2008; Prieto and Dahners 2009; Venner et al. ic competition is not equal, with the former 2011). being the stronger. However, it can almost be the same when species show similar morpho- Another determining factor in community logical characteristics, like it has been shown structure is body size. Resource use (e.g., for some species of Coenagrionidae (Moore prey) depends on the body size of predators 1964; Beukema 2004), Calopterygidae (De and often determines competition with heter- Marchi 1990; Nomakuchi and Higashi 1996; ospecifics. As a result, body size is not Tynkkynen et al. 2004; 2005), and others. randomly distributed among species within the same community, but rather it is evenly In odonates, many congenerics have apparent- spaced (Hutchinson 1959). In other words, ly similar habitat requirements and usually there is a critical size similarity threshold that live in sympatry. These species are a good allows species coexistence (Horn and May model to study interspecific competition and 1977). Otherwise, interspecific competition niche partitioning. In a recent study on the in- would act like a limiting force inducing regu- ventory of adult odonates dwelling in the

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Journal of Insect Science: Vol. 13 | Article 71 Khelifa et al.

crohabitat use of adults of three congeneric dragonfly species, O. chrysostigma, O. co-

erulescens anceps, and O. nitidinerve, were surveyed to discover the ecological mecha-

nisms that maintain their coexistence.

Materials and Methods

The study was undertaken upstream of the Seybouse River in Northeast Algeria at the

Old Bridge canal, which is situated 5 km west Figure 1. Presentation of the study site. 1. Map of the Old of Guelma city (36° 28' N, 7° 22' E). The wa- Bridge canal. 2. Map of the sample area; a, b, c, and d present the sections sampled. Section a and c were open areas while section tercourse is 450 m long, and has an average b and d were covered and high vegetated areas. High quality depth and width of 7 and 120 cm respectively. figures are available online. At its lower part, it splits in two streamlets flowing on both sides of a dense reed for Seybouse watershed in northeast Algeria, about 80 m, which then meet at 30 m from its three species of Orthetrum, the yellow veined outlet to the Seybouse River (Figure 1). To skimmer, Orthetrum nitidinerve Sélys (An- our knowledge, the canal has never been used isoptera: Libellulidae), the Epaulet skimmer, for irrigation. The dominant vegetation at the O. chrysostigma (Burmeister), and the keeled edge of the canal was exclusively shrubs of skimmer, O. coerulescens anceps (Schneider), oleander, Nerium oleander L. (Gentianales: were usually found sharing the same locality Apocynaceae), at its upper region, but the rest during their flight period (Khelifa et al. 2011). was dominated by cattail, Typha angustifolia In a context of ecological niche, these three L. (Poales: Typhaceae), sea rush, Juncus species are quite similar morphologically and maritimus Lamark, and knotgrass, Paspalum behaviorally, share the same resource (territo- distichum L. near its outlet. In addition to the ries in the breeding area that increase the three study species, other species of Odanata breeding success of males), live in the same were also present, including the copper dem- habitat, and at the same time their coexistence oiselle, Calopteryx haemorrhoidalis Vander is almost, or totally, impossible for many the- Linden, the Iberian bluetail, Ischnura graellsii orist biologists (Volterra 1928; MacArthur Rambur, featherleg, Platycnemis subdilatata and Levins 1964; Levin 1986; and others). Sélys, small red damselfly, Ceriagrion ten- However, if these species co-occur in a natu- ellum De Villers, and Mediterranean bluet, ral environment, they must necessarily have, Coenagrion caerulescens Fonscolombe. to some extent, separate niches by at least one axis. Breeding behavior observations Daily observations were made on the breeding Odonates have been well-studied in the field behavior of the three skimmer species from 20 of niche partitioning, but most work has been June to 25 July 2011 in the morning (10:30– focused on the larval stage (Crowley and 12:30) and afternoon (13:30–15:30). Mature Johnson 1982; Dudgeon 1989; Sternberg adults were individually marked on their right 1991, Wissinger 1992; Mahato 2000). In the hind wing with a permanent marker and fol- present study, the breeding behavior and mi- lowed from an observation point at a distance

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Journal of Insect Science: Vol. 13 | Article 71 Khelifa et al. Table 1. Breeding behavior description of the three dragonfly species. Lowercase in acronyms refers to transitional type (Sakagami et al. 1974).

Table 2. Mean ± standard deviation values of abiotic factors for the four sections sampled.

of 3 m. At this position, the observer can both easily detect the conspicuous marks and avoid Body size measurements any disturbance on active individuals. The Mature skimmers (of the three skimmer spe- classification of Sakagami et al. (1974) was cies) were captured by a hand net, marked followed to place each species in its breeding individually by a permanent marker on the behavior category (Table 1). Quantitative data right hind wing and thorax, and some of them (the duration of each behavior component) were measured (the total body length from the were not reported here because they were not head to the end of the abdomen including cer- thought to have a crucial role in the interspe- ci and the left hind wing length) by a digital cific competition intensity. Every dragonfly caliper to the nearest 0.01 mm. species has a complete breeding behavior se- quence that starts with the encounter of the Microhabitat survey two sexes and ends with oviposition. The pur- The three skimmers were not common at the pose of this study was only to highlight upper part of the watercourse, which was potential qualitative (presence or absence) dominated by a large population of C. haem- similarities in the breeding behavior compo- orrhoidalis. Therefore, our study was only nents of the three congeneric species. Since focused on downstream of the canal, limited they were all territorial, and resembled one to approximately 200 m, and divided to 4 sec- another in coloration (for the three species, tions according to the watercourse’s physical mature males and females are blue and brown- characteristics (Table 2) and especially vege- ish-yellow, respectively), it was assumed that tation cover. Section a and c were open areas, an individual of a skimmer species displaying while section b and d were highly vegetated a particular behavior (like oviposition in fe- (covered) areas. Some abiotic factors were males) within a breeding area is more likely to randomly taken from 10 points within each be interfered or intercepted (when it is a fe- section, recording the water width, depth, ve- male) by a male belonging to a different locity, emergent vegetation height and species and have a similar behavior in its spe- density, bank vegetation height and density, cies ethogram. Therefore, the more the and emergent stone density. A quadrat (1 m²) similarities in breeding behavior sequence be- was used to estimate densities. The flight pe- tween species, the stronger the interference riod of O. chrysostigma and O. nitidinerve competition. started in late May, while O. c. anceps adults

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Journal of Insect Science: Vol. 13 | Article 71 Khelifa et al. started to be observed only in early June. The were released after they were able to grasp the investigation was initiated when the three spe- vegetation. By doing so, individuals tended to cies became reproductively active. The spatial stay in the same position. After 15 minutes distribution of the three skimmers was sur- (during which few skimmer individuals en- veyed daily from 10:00 until 16:00 from 12 tered the section), the host section was first June until 28 July 2011 by slowly walking checked and then the 3 remaining sections along the canal and hourly recording the num- were intensely searched for potential marked ber of individuals (males and females) of each individuals, which were recorded in their re- species within each section. Sex was not con- spective position. sidered for further analysis. Immature individuals were not included in the analysis, Statistical analysis because they could bias the results because Most statistical analyses were computed by mature adults could easily influence their dis- SPSS 17.0. To analyze the spatial distribution tribution. For further analysis, only the data, data of sections with similar physical maximum number recorded within a day was and environmental characteristics (Table 2) taken (usually at 12:00). were pulled together after a principal compo- nent analysis (Figure 2, Table 3). In other Translocation experiment words section a with section c, and section b O. c. anceps was the smallest species within with section d for open and covered areas, re- the three studied skimmers, and one might spectively. To compare the number of think that its distribution could be substantial- individual adults counted in open versus cov- ly affected by the two larger ones inducing its ered sections, a Mann-Whitney test was exclusion from its preferred (micro-) habitat. performed using an alpha-value of 0.05. A To examine this, removal and translocation Kruskal-Wallis test was carried out to illus- experiments were done in section c during 3 trate the difference of body and hind wing consecutive days (26–28 July). This section lengths between species (alpha-value = 0.05), was chosen because its small size enabled a and a Dwass–Steel–Chritchlow–Fligner post quite perfect control (see Figure 1.2), and also hoc test was computed for pair-wise compari- no skimmer individual would enter the section sons (Critchlow and Fligner 1991). EcoSim coming from the river through the canal outlet

(Figure 1). This period was also chosen be- cause the numbers of the two larger species

had begun to decrease in late-July, which was advantageous for the experiment. First, each

skimmer was captured and kept in a cage (they were released after the experiment).

Then, 30 marked mature males (10/day) of O. c. anceps coming from section b and d were

translocated to section c. It is important to point out that individuals were not released in

the air because that induced their instant dis- Figure 2. Position of the all samples in a principal component persal out of the section. Instead, they were space using eight environmental variables (water width, water depth, water velocity, emergent vegetation density, emergent taken by the wings, deposited carefully on a vegetation height, bank vegetation density, bank vegetation plant support in the middle of the section, and height, emergent stone density). Samples 1–10 were taken from section a, 11–20 from b, 21–30 from c, and 31–40 from d. High quality figures are available online.

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Journal of Insect Science: Vol. 13 | Article 71 Khelifa et al. Table 3. Principal Component Analysis for the two principal components retained for interpretation. The table presents behavior was not easy to survey, due to dis- Eigenvectors (correlations) for each abiotic factor (values great- turbances produced by conspecifics, other er than 0.40 are in bold), eigenvalues, and percentage of explanation. The two principal components with eigenvalues skimmer species, or cattle crossing the canal. greater than 1 were retained for interpretation. 95.16% of the A total of 102 individuals of O. nitidinerve data variability was explained by the association of the two axes. Water velocity and emergent stone density were negatively (58 females, 44 males), 34 O. chrysostigma correlated with the first principal component, while water vege- (16 females and 18 males), and 53 O. c. an- tation and water vegetation height were positively correlated with the same axis. Water depth and bank vegetation density ceps (19 females and 34 males) were were positively related to the second principal component. individually marked during our survey.

Interspecific interferences were frequent be-

tween males of O. nitidinerve and O. chrysostigma. Contests between O. nitidinerve

and O. c. anceps were less common. Howev- er, males of O. chrysostigma and O. c. anceps

rarely interacted. Attempts for heterospecific pairing were observed between all species. 7.0 software (Gotelli and Entsminger 2001) Pre-copulatory tandems between O. nitidi- was used for the analysis of niche and size nerve males and O. chrysostigma females and overlap. Pianka’s index was used to calculate between O. chrysostigma males and O. c. an- the niche overlap for each pair of species us- ceps females were detected. Although pairs ing microhabitat use data (Pianka 1973). tried to form the copulatory wheel, interspe- Regarding the size overlap analysis, the null cific copulation was never noted. model hypothesis supposes that there is an even interspecific spacing in body size of ad- A summary of the reproductive behavior of jacent species, i.e., the smaller the segment the three species is presented in the Table 1. It length (δ²), the more homogeneity in size rati- was noticed that O. chrysostigma and O. c. os between coexisting congeneric species anceps had the same complete behavioral se- (Gotelli and Illison 2002). Variance in seg- quences, and O. nitidinerve behaved in the ment length metric, the Log uniform same way before copulation but substantially distribution, and Log transformed data were different just after. All the study species were used. territorial. Males remained perched on a sup- port, expressing strong agonistic behavior Results toward any skimmer male (irrespective of species) approaching their territory. Once the Description of the breeding behavior female arrived, males rapidly went in her di- During the study period, observation were rection, intercepted her in the air, and formed made for 175 hours over 35 days, and 39, 31, the pre-copulatory tandem. This state did not and 19 complete breeding behavior sequences last a long time, just few seconds (sometimes of O. nitidinerve, O. chrysostigma, and O. c. 1 sec) before the copulatory wheel establish- anceps were observed, respectively. The low ment. However, pre-copulatory tandems were observation number of the last species was sometimes recorded perched on a support in due to its tendency to copulate at high vegeta- the same state for some minutes. Observations tion cover, which made observation difficult. from marked individuals revealed that those Also, a complete sequence of the reproductive couples were the ones usually chased by other

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Journal of Insect Science: Vol. 13 | Article 71 Khelifa et al.

stayed in an immobile state by holding a sup- port, and wriggled her abdomen from time to

time. Strings of eggs produced by the female were fixed to the support surface, which was

either a plant stem or a stone. On the other hand, the O. chrysostigma and O. c. anceps

male released the female at the perching site and then patrolled and ended up perched next

to her. The female, on the other hand, rested alone at the perching site for a while and then

headed to the oviposition site to lay her eggs, followed closely and synchronously by the

male. The oviposition behavior of both spe- cies was completely different from O.

nitidinerve. She beat the end of her abdomem many times on the water surface in flight and

regularly changed her laying points.

Size overlap The size of the three species was significantly

different (Kruskal-Wallis test for body and hind wing length respectively: χ² = 75.20, df =

2, p < 0.0001; χ² = 73.73, df = 2, p < 0.0001) (Table 4). Multiple comparison revealed that

the size of each species differed significantly Figure 3. Body size overlap patterns for the body and hind from the others (body length: O. nitidinerve > wing length of . Frequencies of simulated variance in segment length (δ²) are shown in the histograms. They give a O. chrysostigma: p < 0.0001; O. nitidinerve > good picture on whether the size ratios between adjacent spe- O. c. anceps: p < 0.0001; O. chrysostigma > cies are stable or not. Arrows point out the observed variances. Values beside arrows are the tail probabilities coupled to the O. c. anceps: p < 0.0001; hind wing length: O. observed variances. High quality figures are available online. nitidinerve > O. chrysostigma: p < 0.0001; O. nitidinerve > O. c. anceps: p < 0.0001; O. males. If copulation is considered to begin chrysostigma > O. c. anceps: p < 0.0001). The when the copulatory wheel occurs, then for two morphological parameters were used to the three species the copulation started in the measure the size overlap between the three air but the majority of its duration was spent at species. For both traits, there were quite large a perching site. variances of segment lengths, indicating that although the three species differed significant- After copulation, the male O. nitidinerve went ly in size, the ratios of adjacent species did not to the oviposition site in copula, hovered appear more evenly spaced than expected by above it with some up-and-down movements chance (Figure 3). Table 4 shows that O. ni- at 20 cm from the water surface, released the tidinerve was the largest species and that O. c. female, and undertook few patrols around her anceps was the smallest. O. chrysostigma and before perching next to her for guarding. The O. c. anceps were the most similar skimmers, female immersed her abdomen in the water, differing only by approximately 2 mm, while

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Journal of Insect Science: Vol. 13 | Article 71 Khelifa et al. Table 4. Body and hind wing length of the three skimmer species. Values represent the mean ± standard deviation. Value between brack- ets is sample size.

the larger O. nitidinerve exceeded them by at respectively). Figure 5 presents the adult pro- least 6 and 8 mm respectively in both body portions of the three skimmers recorded in the and hind wing length (Table 4). two microhabitats. It shows the occurrence of O. chrysostigma and O. nitidinerve in open Spatial distribution areas, and O. c. anceps in covered ones. It Figure 4 reveals that O. chrysostigma was the may inferred that the former species was ex- least abundant species (mean of maximum per clusively confined to open areas, since only 4 day = 1.71), never exceeding 10 individuals. individuals were observed in covered sections The two other species, clearly more abundant during the whole study period. Similarly, O. with 6.10 for O. nitidinerve and 6.64 for O. c. nitidinerve predominately occurred in open anceps, showed a substantial increase in July, sections, but a quite substantial proportion al- especially for the latter. Abrupt and usually so frequented vegetated ones probably synchronous decreases in the three species because its high numbers elicited strong intra- numbers were due to bad weather conditions. specific competition. In fact, a male was often For example, on 25 June, no skimmer individ- observed chasing another one from his territo- ual was recorded because of heavy wind. ry, travelling up to 50 m. The loser of the contest usually perched in peripheral sections. The spatial distribution of the three species On the other hand, O. c. anceps was mainly was not homogeneous along the two micro- located in covered sections, and its occurrence habitat types (U = 258, p < 0.0001; U = 93, p in open ones was generally due to the pres- < 0.0001; U = 117.5, p < 0.0001, for O. nitidi- ence of some small vegetated parts usually nerve, O. chrysostigma, and O. c. anceps, occupied by 1 individual male. Two species, O. nitidinerve and O. chrysostigma, mainly

co-occurred in the same open microhabitat,

Figure 4. Abundance of the three species of dragonfly during Figure 5. Utilization of microhabitats (open and covered) by the study period. Bars represent the number of both sexes. the three skimmer species. Open and filled bars refer to open High quality figures are available online. and covered microhabitats, respectively. High quality figures are available online. Journal of Insect Science | http://www.insectscience.org 8

Journal of Insect Science: Vol. 13 | Article 71 Khelifa et al. Table 5. Pairwise niche overlap between the three skimmer species. closely similar congeneric species living in sympatry. The main question was how conge-

neric species with similar morphology and behavior living in the same system and at the

same time could coexist. Reproductive behav- and one species, O. c. anceps, occupied highly ior, size overlap, and microhabitat use were vegetated microhabitat. investigated to reveal potential biological and ecological isolation between three sympatric Translocation experiment congeneric species of dragonflies (genus Or- The translocation experiment, which moved thetrum). 30 marked individuals (males) of O. c. anceps from covered sections to an open and empty Breeding behavior and ecology of the subspe- (absence of skimmers) one, showed that no cies O. c. coerulescens have been well individual remained at the same host section, documented (Parr 1983; Buchwald 1989; Mil- and 16 returned to the covered ones (three of ler and Miller 1989; Buchwald and Schmidt them were recorded at the same position (ter- 1990; White 2006; White 2008), probably be- ritory) where they had been captured). The cause of its large distribution in the Western remaining 14 individuals were not recovered, Palearctic. Similarly, O. chrysostigma was probably because of their displacement out of also studied extensively in sub-Saharan Africa the canal. Therefore, it can be inferred that the (Miller 1983; Schenk et al. 2004; Koch 2005; smaller (O. c. anceps) species was not exclud- Koch and Suhling 2005; Suhling et al. 2006). ed from open areas by the two larger ones, but However, data regarding O. nitidinerve, a spe- rather simply preferred areas with high vege- cies with a distribution restricted to the tation cover. Mediterranean basin (Dijkstra et al. 2007), are still lacking (Khelifa et al. 2012). Niche overlap Niche overlap estimates using Pianka’s index Similarities in appearance, behavior, and body are presented in Table 5 for the three species size support the view that at least two species pairs. The lowest niche overlap value (0.20) could not live in the same habitat. The three was between O. c. anceps and O. chrysostig- study species belonged to the Orthetrum ge- ma, an intermediate one (0.45) was observed nus and had broadly the same blue coloration. between O. nitidinerve and O. c. anceps, After surveying them during their breeding while the highest (0.96) was between O. ni- season, it was found that two of them, O. c. tidinerve and O. chrysostigma (Table 5). Like anceps and O. chrysostigma, had similar the spatial distribution revealed, the two for- breeding behavior sequences. It has been mer species rarely occupied the same area, shown that coloration (Andrew 1966) and whereas the third species pair consisted of flight pattern (Pajunen 1966) affect visual skimmers with the same microhabitat prefer- recognition of adult so that individu- ences. als can display predatory, agonistic, breeding, or no behavior accordingly. Waage (1975) Discussion showed that two sympatric Calopterygidae, Calopteryx maculata and C. aequabilis, in Our study emphasized the role of habitat het- North America used wing pigmentation to erogeneity in maintaining the coexistence of discriminate between congenerics, but repro-

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Journal of Insect Science: Vol. 13 | Article 71 Khelifa et al. ductive isolation was not absolute, because areas (Baker 1981) and affect larval habitat interspecific copulation often occurred. The use (Suhling 1996; Suutari et al. 2004). Near breeding behavior of O. c. anceps was similar the Indian Ocean, two arboreal day geckos, to that of the subspecies O. c. coerulescens Phelsuma ornata and P. cepediana, shared the reported by Parr (1983), Miller and Miller same tropical (Harmon et al. 2007). (1989), and White (2006), matching also that Removal experiments of the latter species in- of its congeneric O. chrysostigma, which was duced the increase in abundance of the later already investigated by Miller (1983). How- one, which highlighted the effect of interspe- ever, O. nitidinerve had a quite different cific interactions between these two behavior, first described in our study and rare- congenerics. Based on this assumption, our ly observed in dragonflies (Corbet 1999). field experiment was performed to investigate potential shifts in resource utilization (micro- In terms of interspecific interference, O. c. habitat occupancy) of the smaller species (O. anceps was not totally isolated from the two c. anceps) after removal of larger congenerics. other species. Open sections also supported It showed that O. c. anceps preferred highly- small, vegetated patches that could be occu- vegetated areas, and in contrast to the study on pied by an individual mature male. Within a geckos (Harmon et al. 2007), its occurrence in plot of 4 m², for example, the three species that specific microhabitat was not the result of maintained different perching sites and ago- exclusion by larger species. nistic behaviors often took place regardless of size (the smallest could interfer with the larg- The even spacing of body size of species dic- est), as was observed in three coexisting tated by Hutchinson (1959) was not found in species of Leucorrhinia (Singer 1990). Simi- the three species studied when the whole sys- larly, using marked individuals, interspecific tem was considered (excluding habitat pairing was observed, but copulation was nev- heterogeneity), because O. c. anceps and O. er observed, apparently because males had chrysostigma, displaying the same breeding difficulty maintaining the copulatory tandem. behavior, also had quite similar size. Brown Similar observations were recorded between and Wilson (1956) and Hutchinson (1959) Libellula quadrimaculata females and L. de- concluded that coexistence is not possible in pressa males (Paine 1994). It is probable that such a case. Even spacing of morphology and there is a degree of similarity in anal append- body size has been noticed in some insect ages and female prothorax of the three groups, such as Coleopterans (Brandl and congeneric species that enabled heterospecific Topp 1985) and Dipterans (Syrphidae) (Gil- pairing (Pinhey 1963; Lieftinck 1981). In ad- bert et al. 1985). dition, intra- (between males) and intersexual interactions with congenerics suggested a poor Many need territories to increase their recognition between the three dragonfly spe- fitness during the breeding season. Dragon- cies. Such mistaken species recognition was flies show elaborate territorial behavior also reported between two closely related spe- (Corbet 1999). The mature male guards an cies of damselflies, Calopteryx virgo and C. area within a and struggles with other splendens (Tynkkynen et al. 2005). males in order to maintain his territory and reproduce (Corbet 1999). By occupying it, the In Odonata, interspecific interference was individual will reduce the limited resource, shown to exclude conspecifics from foraging which is space, not only for conspecifics but

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Journal of Insect Science: Vol. 13 | Article 71 Khelifa et al. also for heterospecifics with similar morpho- habitat characteristics as those presented by logical traits (color, size, or structural Heymer (1969) for O. brunneum. morphology) and similar habitat preferences. Such cases are common between congenerics It is reasonable to think that sympatric conge- (Warren and Lawton 1987; Juliano and Law- neric species diverge at the microhabitat scale ton 1990). In our study, it was supposed that because they usually exploit local food in the the three species interacted regularly to own same way (Benke and Benke 1975; Joahanns- breeding territories. Since territories are valu- son 1978), which results in the exclusion of able for territorial dragonflies during the the less competitive. For example, in the east- breeding season, a close examination of one ern United States, two congeneric of the three main resources in species ecologi- Zygopterans, Enallagma aspersum and E. tra- cal niche proposed by Schoener (1974), viatum, had different habitat preferences, with namely the microhabitat. the former restricted to small fishless ponds and the latter to ponds with insectivorious fish One of the most common examples of habitat (Pierce et al. 1985). Although spatial isolation partitioning between sympatric congeneric of closely related species is the general pat- species in ecological communities is that of tern, other studies have shown that congeners Caribbean Lizards (Anolis spp), in which spe- and morphologically similar species converge cies use different perching heights and in both time and space (Wissinger 1992; diameters within trees to gain spatial isolation Crowley and Johnson 1982). In the current (Schoener 1975; Losos 1994). During our study, the two species with the same ecologi- study, the spatial distribution survey revealed cal preferences in terms of breeding territories that two species, O. nitidinerve and O. chryso- interacted regularly, and the exclusion of O. stigma, mainly occupied open areas while the chrysostigma by O. nitidinerve was thought to other one, O. c. anceps, occurred in highly- occur. Sokolovska et al. (2002) and Thomp- vegetated (covered) ones. Since niche overlap son and Fincke (2002) reviewed the effect of measure was based on microhabitat use, its body size on territorial odonates’ fitness, and value was highest between O. nitidinerve and they concluded that larger insects mate with O. chrysostigma (0.96), intermediate between more females (higher male mating rate) by O. nitidinerve and O. c. anceps (0.45), and winning more contests with other males. Since lowest between O. chrysostigma and O. c. an- both species were phenotypically alike, the ceps (0.20). Thus, the two species with similar larger species (O. nitidinerve) might potential- sizes and behaviors were spatially isolated. ly win territorial contests more frequently. This could explain the low numbers of the lat- Previous studies conducted on the subspecies ter species during the entire study period. In O. c. coerulescens in Europe reported similar addition, three marked O. chrysostigma ma- habitat preferences to that of O. c. anceps, ture males were recovered in a channel at 300 with vegetated water as the typical suitable m from the canal, but no individual male of habitat (Heymer 1969), but the former sub- the larger species was found to have displaced species is known to frequent other so far. intermediate (Buchwald 1989; Buch- wald and Schmidt 1990; White 2008; We inferred that both spatial heterogeneity Wildermuth 2008;). O. nitidinerve and O. and differential microhabitat preferences chrysostigma had approximately the same could maintain a mixed population of conge-

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Journal of Insect Science: Vol. 13 | Article 71 Khelifa et al. neric species in the same system. We assume that similar patterns of microhabitat prefer- Behangana M, Luiselli L. 2008. Habitat niche ences might occur between the two community-level analysis of an amphibian congeneric species, Orthetrum trinacria and assemblage at Nabugabo, . Web O. sabina, that coexist in the northern limits Ecology 8: 125–134. of the Algerian Sahara (Dijkstra et al. 2007). Our results suggest that the three studied spe- Benke AC, Benke SS. 1975. Comparative dy- cies, especially O. c. anceps, were genetically namics and life histories of coexisting predisposed to choose their respective micro- dragonfly populations. Ecology 56: 302–317. habitats, as is usual in (Jaenike and Holt 1991). Further studies should focus on Beukema JJ. 2004. Recognition of conspecific the larval stage to investigate if: (1) similar females by males of Calopteryx haemorrhoi- spatial patterns also occur during their aquatic dalis (Vander Linden) (Zygoptera: life, (2) strong interspecific competition (ex- Calopterygidae). Odonatologica 33: 147–156. ploitative or interference) or intraguild cannibalism occurs and to what extent, and 3) Brandl R, Topp W. 1985. Size structure of niche axes other than microhabitat act to Pterostichus spp. (Carabidae): aspects of maintain their coexistence. competition. Oikos 44: 234–238.

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