Next Article in Journal
How Old Is a Turtle? Challenges in Interpreting Age Information in Sea Turtles
Previous Article in Journal
Bibliometric Insights into Terrestrial Laser Scanning for Forest Biomass Estimation
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Ecologies
Volume 5
Issue 3
10.3390/ecologies5030030
ecologies-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

The Effect of Age on Survival Is Similar in Males and Females of an Aquatic Insect Species

by
Abdeldjalil Youcefi
1,
Hayat Mahdjoub
2,*,
Rabah Zebsa
3,
Amin Kahalerras
4,
Hichem Amari
5,
Abdelheq Zouaimia
3,
Soufyane Bensouilah
6 and
Rassim Khelifa
2,*
1
Biology Department, University of Tamanrasset, Tamanrasset 11000, Algeria
2
Biology Department, Concordia University, 7141 Sherbrooke St. W., Montreal, QC H4B 1R6, Canada
3
Department of Nature and Life Sciences, Faculty of Nature and Life Sciences and Earth and Universe Sciences, University of 08 May 1945, Guelma 24000, Algeria
4
Direction Générale Des Forêts, Guelma 24000, Algeria
5
Department of Natural Sciences, Ecole Normale Supérieure de Ouargla, Ouargla 30000, Algeria
6
Biology Department, Université de Laghouat, Laghouat 03000, Algeria
*
Authors to whom correspondence should be addressed.
Ecologies 2024, 5(3), 491-501; https://doi.org/10.3390/ecologies5030030
Submission received: 17 July 2024 / Revised: 15 August 2024 / Accepted: 16 August 2024 / Published: 3 September 2024
Browse Figures
Versions Notes

Abstract

:
Age is a critical intrinsic factor that influences the probability of survival of organisms on Earth. In many animals, the lifestyles and habitat occupancy of males and females are so different that the effect of age could be sex-dependent. To reveal such patterns in wild animal populations, we here use a natural population of the Mediterranean demoiselle Calopteryx haemorrhoidalis Vander Linden (Calopterygidae: Zygoptera) in Northeast Algeria to analyze the influence of age and sex on survival probability using daily capture–mark–recapture. We used stepwise model selection on Cormack–Jolly–Seber models that explain recapture and survival probability, including age and sex as covariates. We marked a total of 214 adults throughout the study period (41 days). The sex ratio did not deviate from unity. Recapture probability depended on sex and time, with a slightly higher recapture probability in males (0.30 [95% CI: 0.27–0.35]) than females (0.26 [0.22–0.30]). The survival probability was slightly higher in females (0.89 [0.86–0.91]) than males (0.86 [0.82–0.88]). The best model for the survival probability included an additive effect of sex and age, indicating that the survival probability of both sexes declined with age. Interestingly, the lifespan of some individuals reached 119–130 days, which is surprisingly long compared to other temperate damselflies.

Graphical Abstract

1. Introduction

Empirical studies have documented the effect of age on survival and fecundity in many animal taxa [1,2,3]. One typical age effect is a decrease in survival rate with chronological age [4]. The literature on senescence in wild populations is dominated by studies on vertebrates such as mammals and birds, but invertebrates like insects remain relatively less documented [5]. Studies on senescence have been conducted in some insect groups, including dipterans [6,7], hymenopterans [8], orthopterans [9], and odonates [10,11]. There are various intrinsic and extrinsic factors that could influence the effect of age on individuals. For instance, the magnitude and direction of the effect of age could differ between males and females [12,13], especially in species where sexes differ substantially in lifestyle and habitat use [14,15]. This hypothesis on the differential age effect on sexes warrants investigation in wild populations of insect species with long lifespans.
Odonates are suitable for capture–mark–recapture (CMR) studies because they are relatively easy to capture, mark, and survey throughout their lifespan [16]. Many studies have applied the CMR technique on damselflies to answer ecological and evolutionary questions because they are easy to catch and likely to stay in the same area after release [17,18,19]. The effects of sex and age on the survival rate have been investigated in various studies on damselflies [20]. A recent meta-analysis investigating drivers of survival rate showed that age showed a significant effect, whereas sex did not [20]. This finding confirms the conclusions of Sherratt, Laird, Hassall, Lowe, Harvey, Watts, Cordero-Rivera, and Thompson [10], who found that age-dependent models of survival performed better than those without age dependence at explaining the CMR data on various dragonflies and damselflies. The direction of the effect of age on the survival rate of odonates varied across studies. For instance, in Platycnemis subdilatata Selys, tenerals (recently emerged adults) and immature individuals had lower survival probabilities than mature individuals [21]. Studies on mature damselflies showed that the effect of age was negative [10,22], indicating a lower survival rate in older individuals. Despite the large number of CMR studies, only a few studies have investigated the differential effect of age in males and females [12,13].
Although CJS models are suitable for CMR of odonates, their estimates of apparent survival could be slightly biased due to individual emigration. In fact, the spatial and temporal (season) coverage of the CMR sampling should determine the accuracy of the survival and lifespan estimates [16]. First, a meta-analysis of 39 species showed that the longer the CMR survey, the more accurate the estimate of survival probability [20]. Second, the larger the sampling area, the more likely marked individuals are resighted and the less likely emigration occurs [23]. Thus, to avoid these shortcomings, CMR surveys should be carried out across larger areas and for longer periods. However, most CMR studies have targeted small areas (<1 km transect), and span only a few weeks, which may result in an underestimation of the survival, the lifespan, and the effect of age on survival of individuals.
Calopteryx haemorrhoidalis Vander Linden is a Mediterranean damselfly that is native to North Africa (Algeria, Tunisia, and Morocco) and western Mediterranean Europe (Iberia, Southern France, Italy, and Monaco) [24]. The species is listed as Least Concern in the IUCN Red List. Across its range, the species is very common in various lotic habitats, particularly in rivers and streams. Its flight period is relatively long, from May to September in Europe [25,26] and slightly longer in North Africa (late March to October) [27,28]. The available CMR-based estimates of maximum lifespan of the species are 43 days in Spain [29] and 39 days in France [30]. Compared to other congeneric species that exist across its range (e.g., C. splendens Harris, C. virgo Linnaeus, C. exul Selys), C. haemorrhoidalis has received less research attention. In North Africa, most research on the life history, behavior, and ecology of Calopteryx focuses on the endemic endangered C. exul [31,32,33] and rarely on C. haemorrhoidalis [34]. To our knowledge, capture–mark–recapture studies on C. haemorrhoidalis have been exclusively carried out in Europe [29,30,35,36,37], and not in North Africa.
In this study, we aim to assess the effect of sex and age on the survival of the damselfly C. haemorrhoidalis in the Seybouse River, Northeast Algeria. We used daily CMR from late April to early June across a 2 km stretch of the river. We specifically assessed the seasonal pattern of abundance of the species. Then, using Cormack–Jolly–Seber models, we determined the best model for recapture and survival probability using different covariates that include sex and age. Finally, we reported unusually long lifespans for this species by recording individuals that we marked in summer during the autumn. We hypothesize that age will have a similar effect on males and females because the latter do not typically show spatial segregation at the adult stage even during maturation [29].

2. Materials and Methods

2.1. Study Area

We carried out this study in the Seybouse River, northeastern part of Algeria. The region has a Mediterranean climate (Csa Köppen climate classification) with hot and dry summers and cool and wet winters. The annual rainfall varies between 350 mm upstream and 608 m downstream. The study location was upstream of the Seybouse River, about 5 km west of Guelma city, and at a 210 m elevation (36°28′023.16″ N and 7°22′032.73″ E). The odonate assemblage consisted mainly of C. exul, C. haemorrhoidalis Vander Linden, Platycnemis subdilatata Selys, and Gomphus lucasii Selys. C. exul and Platycnemis subdilatata were more abundant than C. haemorrhoidalis [38]. The bank vegetation was dominated by Typha angustifolia L., Cyperus longus L., Juncus maritimus Lam., and Paspalum distichum L. Weather data (daily minimum, mean, and maximum temperature) were obtained from a weather station 8 km away from the study site (Belkhir province, Guelma).

2.2. Capture–Mark–Recapture Protocol

To assess the survival probability of C. haemorrhoidalis, we conducted daily capture–mark–recapture on adults across a stretch of 2 km from 27 April (the start of the flight season) to 7 June 2011. The sampling started at 9:30 h and ended at 16:00 h. Some sections of the river were not accessible because of the dense bank vegetation (mainly dense trees of T. gallica). Thus, we divided the river into 10 sections that were visited daily for marking and recaptures. Adults were captured with a hand net, then marked with a permanent marker. We used an alphanumeric code to give an individual mark for each adult (Figure 1). We categorized the age of individuals at first capture, using morphological features (rigidity of the wings and body, body coloration, and presence of pink color in the underside of the few last abdominal segments of the males), into three age classes: teneral (<24 h), immature, and mature. We released the marked individuals at the same locations by gently depositing them on the bank vegetation. Those individuals were not captured again, but just resighted on subsequent sampling occasions. Because the estimation of adult abundance on every occasion was challenging, we used a proxy which consisted of summing the number of newly marked individuals and the number of recaptured individuals. Those estimates were used to assess the seasonal pattern of abundance.

2.3. Capture–Mark–Recapture Modeling

We used the capture–mark–recapture data to design a capture–recapture history for each marked individual, which is a series of consecutive sampling occasions (days) with 1s (presence) and 0s (absence or non-detection) [39]. A capture–recapture history of “1101” means that the individual was captured on the first occasion, resighted on the second occasion, not detected on third occasion, and resighted again on the fourth occasion. We used CJS models to analyze our CMR data [40]. This model estimates two main parameters: recapture probability (p), which is the probability that a marked damselfly (alive) is resighted again during subsequent sampling occasions; and apparent survival probability (Phi), which is the probability that the marked damselfly (alive) survived (and has not emigrated) from occasion t to t + 1.
We designed candidate models for both p and Phi, starting with the simplest model (Phi(.) p (.)) that assumes that both parameters are constant. To determine the best model for p, we set Phi as constant and varied p with time, sex, daily average temperature (temp), and age class (age class at first capture). We gradually increased the complexity of the models by adding more covariates to the model. We used additive models such as Phi(.) p (time + sex + temp + age class). We also included two-way interactions between time and sex, as these were recorded in previous studies [12,20]. We performed model selection using the corrected Akaike criterion (AICc) [41]. We selected the most parsimonious model from the list of models that has ΔAICc < 2. After determining the best model for p, we fixed it in the CJS model and varied Phi with sex, time, age class, and age (age since the first capture). We used both the linear (age) and quadratic terms for age (age2) to assess the potential complex effect of age on survival rate. We used increasingly complex additive models, going from the least complex (p(.)) to the most complex (time + sex + temp + age class + age + age2). Because age could have different effects on males and females, we also tested for the two-way interaction between age and sex.

2.4. Lifespan

In autumn 2011, during a study on Chalcolestes viridis Vander Linden [42] in a nearby stream (1 km away) that flows into the Seybouse River (36°28′18″ N, 7°22′18″ E), we resighted the marked individuals from our CMR of C. haemorrhoidalis. This wetland is a small stream, 7 cm deep and 120 cm wide. The banks are dominated by bushes of Oleander trees (Nerium oleander L). At this time of the year, the odonate assemblage consisted mostly of C. viridis, C. haemorrhoidalis, P. subdilatata, and Orthetrum chrysostigma Burmeister. The watercourse was surveyed from 09:00 to 17:00.

2.5. Statistical Analyses

All our statistical analyses were carried out using R 4.3.1 [43]. We used the RMark 3.0.0 package [44] to analyze CMR data. To determine whether the seasonal distribution differed between males and females, we computed a two-sample Kolmogorov–Smirnov test. We used the MASS package [45] to compute a negative binomial model that assesses the seasonal pattern of abundance in males and females. The model included sex and the linear and quadratic term of Julian date to account for the typical hump-shaped seasonal distribution of adults [46]. We used the DHARMa package [47] to check the goodness of fit of our model. To assess the goodness of fit of our CJS model, we used the release.gof function from the RMark package, which computes three tests (TEST2, TEST3, and TEST2 + TEST3) that test whether the data meet the assumptions of the model [48]. Values are mean ± SD.

3. Results

A total of 214 individuals were captured and marked during the study period. The sex ratio of the captured individuals was 50% (107 males and 107 females). A total of 131 (61.2%) were recaptured at least once. Males were recaptured on average 2.85 ± 2.09 times with a maximum of 15. Similarly, females were recaptured on average 2.78 ± 2.75 times with a maximum of 10.

3.1. Seasonal Pattern of Abundance

The average number of adults recorded across sampling occasions did not differ between sexes (negative binomial: z = 0.33, p = 0.74). There was an average of 7.82 ± 6.76 females and 8.03 ± 4.79 males recorded across the study period. Although abundance fluctuated across sampling occasions, the overall seasonal pattern was hump-shaped (negative binomial: Julian date, z = 5.07, p < 0.0001; Julian date2, z = −5.27, p < 0.0001), with an increase early in the season (late April–early May), then a decline later in the season (late May and early June) (z = −5.80, p < 0.0001) (Figure 2). Males and females had significantly different seasonal distributions of adult abundance (D = 0.135, p = 0.004). The average abundance in the first week of sampling (late April–early May) was 9.80 ± 5.81 males and 4.83 ± 3.19 females, and in the last week of sampling (early June) it was 2.00 ± 1.00 males and 3.00 ± 2.35 females.

3.2. Cormack–Jolly–Seber Model

The goodness-of-fit tests showed no significance (p = 0.99–1; Table S1); thus, the CJS model is suitable for our data. The average recapture rate based on a constant model was 0.28 [0.25–0.31]. We obtained two models with ΔAICc < 2, but the most parsimonious model included the additive effect of sex and time (Table 1). Recapture probability was on average slightly higher in males (0.30 [0.27–0.35]) than females (0.26 [0.22–0.30]). However, across the season, the recapture rate showed marked fluctuations (Figure 3).
The average survival rate based on a constant model was 0.87 [0.85–0.88]. The top model for survival included an additive effect of sex and age (Table 2), revealing that age influenced males and females similarly. Survival probability was on average slightly higher in females (0.89 [0.86–0.91]) than males (0.86 [0.82–0.88]). Our best model predicts that survival rate increases with age in both sexes (Figure 4). Survival models that included age class at capture were not ranked high, indicating that the age classes at capture had relatively similar probabilities of mortality.

3.3. Lifespan

While the expected lifespan based on our CJS model was 6.6 [5.0–7.8] days for males and 8.6 [6.6–10.6] days for females, we resighted three marked males and one marked female in September from our CMR survey in a nearby stream. The estimated lifespans (number of days since marking) were 130, 130, and 119 days. While one of the adults showed notable wearing of the wings, the other two did not.

4. Discussion

Our study investigated the effect of sex and age on the survival of adults of C. haemorrhoidalis, a widespread species in the lotic habitats of North Africa. The species had an equal sex ratio and a relatively asynchronous flight period. Recapture rate depended on sex and time, with males being more likely to be resighted than females. Survival probability was slightly higher in females, and showed a positive age dependence in both sexes. Interestingly, some of our marked males were recorded in the autumn, suggesting that the lifespan of the species could exceed four months.
As expected from previous studies documenting the long flight season of the species in North Africa [27,28,49], our records of the abundance of C. haemorrhoidalis throughout the season suggest that the species has an asynchronous flight period. The flight season started in late April, which is similar to the phenology recorded in other studies in North Africa [34,49] but earlier than that reported in Spain [26]. The species emerged at the same time as its sympatric congeneric C. exul [32] and Gomphus lucasii [50].
Our estimate of the proportion of recaptured individuals (61.2%) was higher than that estimated in Northwest Spain (48%) [29], suggesting that our marked individuals were less likely to leave the sampling area or were more readily detectable (e.g., because of vegetation structure, access to the watercourse). Unlike other studies on damselflies showing a male-biased sex ratio at the adult stage [20,51], our study showed no clear sex bias. The congeneric C. exul, which shows similar reproductive behavior, also exhibits no deviation in the sex ratio from 1:1 [52]. This could be explained by an equal sex ratio at emergence, a relatively similar survival rate during maturation (as we found here with the non-significance of age class on survival rate), and similar habitat use at the adult stage [32]. In territorial species like Calopteryx spp., males guard territories (patches of vegetation) where females aggregate to lay eggs, whereas non-territorial males and non-reproductive females perch on the bank vegetation farther from territories [53]. Thus, due to the lack of spatial segregation between sexes which often leads to a biased sex ratio [14], a transect across the watercourse results in an equal sex ratio. It is important to note that the decline in the abundance of the species in early June was at least partly due to flooding caused by dam water releases that affected the structure of the river in early June. In a study on C. exul on the same site and in the same year, flooding reduced the recapture rate of adults [54], suggesting emigration to other areas.
The recapture probability varied with sex and time. Various studies using capture–mark–recapture on different species found that recapture rate depends on sex and time [21,55,56]. Males often have a higher probability of recapture than females because they are more conspicuous morphologically and behaviorally. In C. haemorrhoidalis, the difference in recapture rate was relatively small, which is most likely due to the lack of spatial segregation (e.g., females remain near the water even for foraging). Recapture rate changes from one day to another, most likely due to weather conditions [12]. Adults are more likely to be active when the weather is optimal (warm and sunny) [46].
The survival probability depended on sex and age, two covariates that studies have shown to influence survival in odonates [20]. In this study, the survival probability of C. haemorrhoidalis was 0.89 in females and 0.86 in males, which is relatively similar to that recorded in a population in Italy (0.84 in males and 0.86 in females) [36]. However, this was slightly lower than the average survival rate estimated for odonates (0.895 for males and 0.898 for females) [20]. A relatively similar survival rate between males and females was observed in Calopterygidae [20]. Our observed higher survival rates in females could be due to the higher activity of males, who have a more conspicuous phenotype and exhibit territorial behavior (males interact with both males and females whereas females interact mostly with males), which could make them more likely to be detected by predators [57].
We did not find an effect of age class at capture on survival rate (teneral, immature, and mature individuals had similar survival rates), which is different than other studies on other damselflies [21]. This could be due to the similarity in habitat use across age classes (all age classes remain near the watercourse), a behavior that was also recorded in a Spanish population [29]. However, the similarity in survival rate among age classes at capture should remove potential biases in the chronological pattern of survival rates across continuous age since capture. Our best model for survival probability, however, included an additive effect of age (days since marking) and sex. This model predicted that the survival rate of males and females increased gradually with age in a similar manner, which confirms our prediction. This finding is different than those found for the damselfly C. puella [10], the honeybee Apis mellifera L. [8], the cricket Teleogryllus commodus Walker [13], and the neriid fly Telostylinus angusticollis Cresson [7], which showed a decline in survival rate with age. Our finding was similar to that recorded on the same species in one of the years of sampling [12]. One possible explanation for the observed increase in survival rate is an improvement in the environmental conditions with the season (abiotic and/or biotic conditions were better later in life). However, the absence of a decline in survival rate later in life is likely due to the long lifespan of C. haemorrhoidalis, which was not fully surveyed by our sampling.
Estimating the lifespan of odonates accurately in natural conditions is difficult because species can disperse due to environmental changes. Our CJS model yielded an expected lifespan of 6.6 [5.0–7.8] days for males and 8.6 [6.6–10.6] days for females, which is slightly lower than the expected lifespans of a Spanish population (10.6 days in males and 12.0 days in females), C. maculata Beauvois (11 days) [58], and Mnais pruinosa Selys (10.7 days) [59]. Nevertheless, our estimate of survival might be an underestimate because the CJS model estimates the apparent survival, which does not distinguish between emigration and mortality [39]. Two months after the end of our CMR survey, while visiting a nearby stream, we recorded three of our marked males, revealing that they were able to survive for more than four months (up to 130 days). These estimates are more than three times longer than those reported for the species ([29], max = 43 days in Spain; [30], max = 39 days in France). This is most likely the longest lifespan for the species and the family [20]. We are not sure whether this extended lifespan is specific to the North African region. Currently, it is difficult to have a clear account because studies on adult odonates that span multiple months are rare to non-existent [20]. One hypothesis to explain this long lifespan is that the local climate in North Africa is more favorable for the species to survive and reproduce compared to Europe. Another hypothesis is that a longer lifespan provides an evolutionary advantage in a climate where drought is common because adults can secure reproduction whenever the hydrological conditions are optimal [60]. The adaptive significance of this long lifespan needs further investigation.
This study is an important contribution to our understanding of the life history of C. haemorrhoidalis in its southern edge where the species has not attracted research attention. Future studies should investigate the frequency of prolonged lifespans in terms of space (geographic range) and time (season). Such a study could be easily carried out given the large abundance of the species in lotic habitats across its range and the relatively long flight season [25]. Given the widespread distribution of the species across elevations, it is worthwhile to assess whether the life history in general, and adult lifespan in particular, shows an elevational gradient.

Supplementary Materials

The following supporting information can be downloaded at https://www.mdpi.com/article/10.3390/ecologies5030030/s1: Supplementary Material: Table S1: Goodness-of-fit tests for the Cormack–Jolly–Seber model of the analysis of capture–mark–recapture data of Calopteryx haemorrhoidalis in the Seybouse River.

Author Contributions

Conceptualization, R.K., H.M.; methodology, A.Y., R.K.; formal analysis, A.Y., R.K., H.M.; investigation, A.Y., R.K.; R.Z., A.K., H.A., A.Z., S.B.; data curation, R.Z., A.K., H.A., A.Z., S.B.; writing—original draft preparation, R.K., H.M., A.Y.; writing—review and editing, R.K., H.M., A.Y., R.Z., A.K., H.A., A.Z., S.B. All authors have read and agreed to the published version of the manuscript.

Funding

RK is supported by a NSERC CRC Tier 2 (CRC-2022-00134) and an NSERC Discovery Grant (RGPIN-2024-04564).

Institutional Review Board Statement

Not applicable.

Data Availability Statement

Data supporting the reported results will be made available upon request.

Acknowledgments

We are grateful to the students who helped us in the preparation and implementation of the capture–mark–recapture study. We give special thanks to Nasr Eddin Sekrane for driving us out to the field site.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. Sherratt, T.N.; Wilkinson, D.M. Big Questions in Ecology and Evolution; Oxford University Press: Oxford, UK, 2009. [Google Scholar]
  2. Stearns, S.C. The Evolution of Life Histories; Oxford University Press: Oxford, UK, 1992. [Google Scholar]
  3. Péron, G.; Crochet, P.A.; Choquet, R.; Pradel, R.; Lebreton, J.D.; Gimenez, O. Capture–recapture models with heterogeneity to study survival senescence in the wild. Oikos 2010, 119, 524–532. [Google Scholar] [CrossRef]
  4. Brunet-Rossinni, A.K.; Austad, S.N. Senescence in wild populations of mammals and birds. In Handbook of the Biology of Aging; Austad, S.N., Masoro, E.J., Eds.; Academic Press: Burlington, MA, USA, 2006; pp. 243–266. [Google Scholar]
  5. Kirkwood, T.B.; Austad, S.N. Why do we age? Nature 2000, 408, 233–238. [Google Scholar] [CrossRef]
  6. Bonduriansky, R.; Brassil, C. Reproductive ageing and sexual selection on male body size in a wild population of antler flies (Protopiophila litigata). J. Evol. Biol. 2005, 18, 1332–1340. [Google Scholar] [CrossRef] [PubMed]
  7. Kawasaki, N.; Brassil, C.E.; Brooks, R.C.; Bonduriansky, R. Environmental effects on the expression of life span and aging: An extreme contrast between wild and captive cohorts of Telostylinus angusticollis (Diptera: Neriidae). Am. Nat. 2008, 172, 346–357. [Google Scholar] [CrossRef] [PubMed]
  8. Dukas, R. Mortality rates of honey bees in the wild. Insectes Sociaux 2008, 55, 252–255. [Google Scholar] [CrossRef]
  9. Zajitschek, F.; Bonduriansky, R.; Zajitschek, S.R.; Brooks, R.C. Sexual dimorphism in life history: Age, survival, and reproduction in male and female field crickets Teleogryllus commodus under seminatural conditions. Am. Nat. 2009, 173, 792–802. [Google Scholar] [CrossRef]
  10. Sherratt, T.; Laird, R.; Hassall, C.; Lowe, C.; Harvey, I.; Watts, P.; Cordero-Rivera, A.; Thompson, D. Empirical evidence of senescence in adult damselflies (Odonata: Zygoptera). J. Anim. Ecol. 2010, 79, 1034–1044. [Google Scholar] [CrossRef]
  11. Khelifa, R.; Mahdjoub, H.; Aouaouche, M.S.; Houhamdi, M. Reproductive behaviour of a North African endemic damselfly, Platycnemis subdilatata (Odonata: Platycnemididae) and probable senescence effects. Int. J. Odonatol. 2016, 19, 157–167. [Google Scholar] [CrossRef]
  12. Hassall, C.; Sherratt, T.N.; Watts, P.C.; Thompson, D.J. Live fast, die old: No evidence of reproductive senescence or costs of mating in a damselfly (Odonata: Zygoptera). J Anim. Ecol. 2015, 84, 1542–1554. [Google Scholar] [CrossRef]
  13. Zajitschek, F.; Brassil, C.E.; Bonduriansky, R.; Brooks, R.C. Sex effects on life span and senescence in the wild when dates of birth and death are unknown. Ecology 2009, 90, 1698–1707. [Google Scholar] [CrossRef]
  14. Stoks, R. Male-biased sex ratios in mature damselfly populations: Real or artefact? Ecol. Entomol. 2001, 26, 181–187. [Google Scholar] [CrossRef]
  15. Beirinckx, K.; Van Gossum, H.; Lajeunesse, M.J.; Forbes, M.R. Sex biases in dispersal and philopatry: Insights from a meta-analysis based on capture-mark-recapture studies of damselflies. Oikos 2006, 113, 539–547. [Google Scholar] [CrossRef]
  16. Cordero-Rivera, A.; Stoks, R. Mark-recapture studies and demography. In Dragonflies and Damselflies: Model Organisms for Ecological and Evolutionary Research; Córdoba-Aguilar, A., Ed.; Oxford University Press: Oxford, UK, 2008; pp. 7–20. [Google Scholar]
  17. Stoks, R.; Córdoba-Aguilar, A. Evolutionary ecology of Odonata: A complex life cycle perspective. Annu. Rev. Entomol. 2012, 57, 249–265. [Google Scholar] [CrossRef]
  18. Corbet, P.S. Biology of odonata. Annu. Rev. Entomol. 1980, 25, 189–217. [Google Scholar] [CrossRef]
  19. Waller, J.T.; Svensson, E.I. Body size evolution in an old insect order: No evidence for Cope’s Rule in spite of fitness benefits of large size. Evolution 2017, 71, 2178–2193. [Google Scholar] [CrossRef] [PubMed]
  20. Sanmartín-Villar, I.; Cordero-Rivera, A. Odonata survival: Insights from mark-recapture experiments. In Dragonflies and Damselflies: Model Organisms for Ecological and Evolutionary Research; Córdoba-Aguilar, A., Beatty, C., Bried, J., Eds.; Oxford University Press: Oxford, UK, 2022; pp. 129–140. [Google Scholar]
  21. Khelifa, R.; Mahdjoub, H.; Baaloudj, A.; Cannings, R.A.; Samways, M.J. Remarkable population resilience in a North African endemic damselfly in the face of rapid agricultural transformation. Insects 2021, 12, 353. [Google Scholar] [CrossRef]
  22. La Porta, G.; Goretti, E. Investigation on the declining Southern Damselfly (Coenagrion mercuriale, Odonata) in a Mediterranean population: Survival rate and population size. J. Insect Conserv. 2019, 23, 667–675. [Google Scholar] [CrossRef]
  23. Conrad, K.; Willson, K.; Harvey, I.; Thomas, C.; Sherratt, T. Dispersal characteristics of seven odonate species in an agricultural landscape. Ecography 1999, 22, 524–531. [Google Scholar] [CrossRef]
  24. Clausnitzer, V. Calopteryx haemorrhoidalis. The IUCN Red List of Threatened Species 2018: E.T158695A75085099. 2009. Available online: https://www.iucnredlist.org/species/158695/75085099 (accessed on 17 March 2024).
  25. Dijkstra, K.-D.; Schröter, A. Field Guide to the Dragonflies of Britain and Europe; Bloomsbury Publishing: London, UK, 2020. [Google Scholar]
  26. Maynou, X.; Martín, R. Phenology of the Odonata assemblage in a Mediterranean stream in the north-eastern Iberian Peninsula. Odonatologica 2019, 48, 27–48. [Google Scholar]
  27. Jacquemin, G.; Boudot, J.P. Les libellules (odonates) du Maroc; Société Francaise d’Odonatologie: Bois d’Arcy, France, 1999. [Google Scholar]
  28. Khelifa, R.; Youcefi, A.; Kahlerras, A.; Al Farhan, A.; Al-Rasheid, K.A.; Samraoui, B. L’odonatofaune (Insecta: Odonata) du bassin de la Seybouse en Algérie: Intérêt pour la biodiversité du Maghreb. Revue d’écologie 2011, 66, 55–66. [Google Scholar] [CrossRef]
  29. Cordero, A. Estructura de tres comunidades de Calopteryx (Odonata: Calopterygidae) con diferente composición específica. Limnética 1989, 5, 83–91. [Google Scholar] [CrossRef]
  30. Heymer, A. Comportements Social et Territorial des Calopterygidae [Odon. Zygoptera]. Ann. Soc. Entomol. Fr. 1972, 8, 3–53. [Google Scholar] [CrossRef]
  31. Khelifa, R. Flight period, apparent sex ratio and habitat preferences of the Maghribian endemic Calopteryx exul Selys, 1853 (Odonata: Zygoptera). Revue d’Ecologie (La Terre et La Vie) 2013, 68, 37–45. [Google Scholar] [CrossRef]
  32. Khelifa, R. Partial bivoltinism and emergence patterns in the North African endemic damselfly Calopteryx exul: Conservation implications. Afr. J. Ecol. 2017, 55, 145–151. [Google Scholar] [CrossRef]
  33. Mellal, M.K.; Bensouilah, M.; Houhamd, M.; Khelifa, R. Reproductive habitat provisioning promotes survival and reproduction of the endangered endemic damselfly Calopteryx exul. J. Insect Conserv. 2018, 22, 563–570. [Google Scholar] [CrossRef]
  34. Benchalel, W.; Beddiar, M.; Boucetta, S.; Bouslama, Z. Bioecology of calopteryx haemorrhoidalis (Zygoptera, odonata) in response to environmental factors in the brabtia sector streams, el-kala, algeria: Implications for ecohydrological biomonitoring. Studia Universitatis” Vasile Goldis” Arad. Seria Stiintele Vietii (Life Sci. Ser.) 2020, 30, 21–32. [Google Scholar]
  35. Córdoba-Aguilar, A. Wing pigmentation in territorial male damselflies, Calopteryx haemorrhoidalis: A possible relation to sexual selection. Anim. Behav. 2002, 63, 759–766. [Google Scholar] [CrossRef]
  36. Cordero, A. Forced copulations and female contact guarding at a high male density in a calopterygid damselfly. J. Insect Behav. 1999, 12, 27–37. [Google Scholar] [CrossRef]
  37. Heymer, A. Étude du Comportement Reproducteur et Analyse des Mécanismes Déclencheurs Innés (Mdi) Optiques chez les Calopterygidae [Odon. Zygoptera]. Ann. Soc. Entomol. Fr. 1973, 9, 219–255. [Google Scholar] [CrossRef]
  38. Khelifa, R.; Mellal, M.K.; Zouaimia, A.; Amari, H.; Zebsa, R.; Bensouilah, S.; Laouar, A.; Houhamdi, M. On the restoration of the last relict population of a dragonfly Urothemis edwardsii Selys (Libellulidae: Odonata) in the Mediterranean. J. Insect Conserv. 2016, 20, 797–805. [Google Scholar] [CrossRef]
  39. Cooch, E.; White, G. Program MARK: A Gentle Introduction. 2006. Available online: http://www.phidot.org/software/mark/docs/book (accessed on 26 April 2024).
  40. Lebreton, J.-D.; Burnham, K.P.; Clobert, J.; Anderson, D.R. Modeling survival and testing biological hypotheses using marked animals: A unified approach with case studies. Ecol. Monogr. 1992, 62, 67–118. [Google Scholar] [CrossRef]
  41. Burnham, K.P.; Anderson, D.R. Multimodel inference: Understanding AIC and BIC in model selection. Sociol. Methods Res. 2004, 33, 261–304. [Google Scholar] [CrossRef]
  42. Kahalerras, A.; Boucenna, N.; Bensakhri, Z.; Boukhamza, M.; Houhamdi, M. No evidence of body size effects on the reproductive behaviour of a non-territorial damselfly Chalcolestes viridis. Zool. Ecol. 2020, 30, 1–10. [Google Scholar] [CrossRef]
  43. R Development Core Team. R: A Language and Environment for Statistical Computing; R Foundation for Statistical Computing: Vienna, Austria, 2024. [Google Scholar]
  44. Laake, J.L. RMark: An R Interface for Analysis of Capture-Recapture Data with MARK. Alaska Fish. Sci. Cent., NOAA, Natl. Mar. Fish. Serv. 2013, 25. Available online: http://www.afsc.noaa.gov/Publications/ProcRpt/PR2013-01.pdf (accessed on 20 January 2024).
  45. Venables, W.N.; Ripley, B.D. Random and mixed effects. In Modern Applied Statistics with S; Springer: New York, NY, USA, 2002; pp. 271–300. [Google Scholar]
  46. Corbet, P.S. Dragonflies: Behaviour and Ecology of Odonata; Harley Books: Colchester, UK, 1999. [Google Scholar]
  47. Hartig, F. DHARMa: Residual Diagnostics for Hierarchical (Multi-Level/Mixed) Regression Models. R Package Version 0.4.6. 2022. Available online: https://cran.r-project.org/web/packages/DHARMa/vignettes/DHARMa.html (accessed on 20 January 2024).
  48. Choquet, R.; Lebreton, J.D.; Gimenez, O.; Reboulet, A.M.; Pradel, R. U-CARE: Utilities for performing goodness of fit tests and manipulating capture–recapture data. Ecography 2009, 32, 1071–1074. [Google Scholar] [CrossRef]
  49. Jödicke, R.; Arlt, J.; Kunz, B.; Lopau, W.; Seidenbusch, R. The Odonata of Tunisia. Int. J. Odonatol. 2000, 3, 41–71. [Google Scholar] [CrossRef]
  50. Zebsa, R.; Khelifa, R.; Kahalerras, A. Emergence pattern, microhabitat choice, and population structure of the Maghribian endemic Gomphus lucasii Selys, 1849 (Odonata: Gomphidae) in northeastern Algeria. Aquat. Insects 2014, 36, 245–255. [Google Scholar] [CrossRef]
  51. Cordero-Rivera, A.; Núñez, J.; Suriel, C. Let’s wait for the evening: Nocturnal copulation in a tropical damselfly Phylolestes ethelae (Odonata, Synlestidae). Anim. Biodivers. Conserv. 2024, 47, 19–32. [Google Scholar] [CrossRef]
  52. Mahdjoub, H.; Zebsa, R.; Kahalerras, A.; Amari, H.; Bensouilah, S.; Samways, M.J.; Khelifa, R. Condition-dependent survival and movement behavior in an endangered endemic damselfly. Sci. Rep. 2023, 13, 21819. [Google Scholar] [CrossRef]
  53. Córdoba-Aguilar, A.; Cordero-Rivera, A. Evolution and ecology of Calopterygidae (Zygoptera: Odonata): Status of knowledge and research perspectives. Neotrop. Entomol. 2005, 34, 861–879. [Google Scholar] [CrossRef]
  54. Khelifa, R.; Mahdjoub, H.; Baaloudj, A.; Cannings, R.A.; Samways, M.J. Effects of both climate change and human water demand on a highly threatened damselfly. Sci. Rep. 2021, 11, 7725. [Google Scholar] [CrossRef]
  55. Khelifa, R.; Zebsa, R.; Amari, H.; Mellal, M.K.; Mahdjoub, H. Field estimates of fitness costs of the pace-of-life in an endangered damselfly. J. Evol. Biol. 2019, 32, 943–954. [Google Scholar] [CrossRef] [PubMed]
  56. Anholt, B.R.; Vorburger, C.; Knaus, P. Mark-recapture estimates of daily survival rates of two damselflies (Coenagrion puella and Ischnura elegans). Can. J. Zool. 2001, 79, 895–899. [Google Scholar] [CrossRef]
  57. Johnson, C. Polymorphism and natural selection in Ischnuran damselflies. Evol. Theory 1975, 1, 81–90. [Google Scholar]
  58. Waage, J.K. Reproductive behavior and its relation to territoriality in Calopteryx maculata (Beauvois)(Odonata: Calopterygidae). Behaviour 1973, 47, 240–256. [Google Scholar] [CrossRef]
  59. Higashi, K. Length of maturation period and daily food consumption of immature damselfly, Mnais pruinosa pruinosa Selys (Zygoptera: Calopterygidae). Tombo 1982, 25, 23–26. [Google Scholar]
  60. Dijkstra, K.-D.B.; Monaghan, M.T.; Pauls, S.U. Freshwater biodiversity and aquatic insect diversification. Annu. Rev. Entomol. 2014, 59, 143–163. [Google Scholar] [CrossRef]
Ecologies 05 00030 g001
Figure 1. A reproductive pair of marked Calopteryx haemorrhoidalis in the Seybouse River (2011).
Figure 1. A reproductive pair of marked Calopteryx haemorrhoidalis in the Seybouse River (2011).
Ecologies 05 00030 g001
Ecologies 05 00030 g002
Figure 2. Temporal pattern of Calopteryx haemorrhoidalis adult males (M) and females (F).
Figure 2. Temporal pattern of Calopteryx haemorrhoidalis adult males (M) and females (F).
Ecologies 05 00030 g002
Ecologies 05 00030 g003
Figure 3. Recapture probability of Calopteryx haemorrhoidalis adult males (M) and females (F) across the season. Error bars are 95% confidence intervals.
Figure 3. Recapture probability of Calopteryx haemorrhoidalis adult males (M) and females (F) across the season. Error bars are 95% confidence intervals.
Ecologies 05 00030 g003
Ecologies 05 00030 g004
Figure 4. Survival probability of Calopteryx haemorrhoidalis adult males (M) and females (F) across age. Error bars are 95% confidence intervals.
Figure 4. Survival probability of Calopteryx haemorrhoidalis adult males (M) and females (F) across age. Error bars are 95% confidence intervals.
Ecologies 05 00030 g004
Table 1. Model selection of the Cormack–Jolly–Seber model assessing the recapture probability. The survival probability was fixed to a constant model (Phi(~.)). Models are ranked based on their AICc (from lowest to highest values).
Table 1. Model selection of the Cormack–Jolly–Seber model assessing the recapture probability. The survival probability was fixed to a constant model (Phi(~.)). Models are ranked based on their AICc (from lowest to highest values).
ModelnparAICcΔAICcWeightDeviance
Phi(~.)p(~Sex + time)412012.90.0000.5631580.2
Phi(~.)p(~Sex + time + Tempc)422015.22.3170.1771580.2
Phi(~.)p(~Sex + time + Age_class)432016.13.1820.1151578.8
Phi(~.)p(~time)402016.23.2630.1101585.8
Phi(~.)p(~Sex + Tempc + time + Age_class)442018.45.5170.0361578.8
Phi(~.)p(~Sex * time)792046.333.4270.0001519.2
Phi(~.)p(~Sex * time + Tempc)802049.036.1020.0001519.2
Phi(~.)p(~Sex * Time)52071.058.0600.0001716.4
Phi(~.)p(~Sex + Time)42073.260.3150.0001720.7
Phi(~.)p(~Time)32074.361.3620.0001723.8
Phi(~.)p(~Sex)32081.168.2140.0001730.6
Phi(~.)p(~.)22082.269.2670.0001733.7
Phi(~.)p(~Sex + Tempc)42083.070.0580.0001730.5
Phi(~.)p(~Tempc)32084.171.1570.0001733.6
Phi(~.)p(~Sex + Age_class)52085.172.1970.0001730.6
Phi(~.)p(~Age_class)42086.073.0790.0001733.5
Phi(~.)p(~Sex + Age_class + Tempc)62086.974.0380.0001730.4
Age_class: age class at capture (teneral, immature, and mature); Tempc: average daily temperature (centered). The dot (.) refers to a constant model. The best model is highlighted in bold.
Table 2. Model selection of the Cormack–Jolly–Seber model assessing the survival probability. The recapture probability was fixed to the best model (p(~time+sex)) (see Table 1). Models are ranked based on their AICc (from lowest to highest values).
Table 2. Model selection of the Cormack–Jolly–Seber model assessing the survival probability. The recapture probability was fixed to the best model (p(~time+sex)) (see Table 1). Models are ranked based on their AICc (from lowest to highest values).
ModelnparAICcΔAICcWeightDeviance
Phi(~Sex * Age)p(~Sex + time)442005.60.0000.4531565.9
Phi(~Sex + Age)p(~Sex + time)432007.61.9890.1681570.2
Phi(~Sex * Age + Sex * Age2)p(~Sex + time)462007.92.3430.1401563.6
Phi(~Sex * Age_class + Sex * Age)p(~Sex + time)482009.03.4610.0801559.9
Phi(~Sex + Age_class + Age)p(~Sex + time)452009.43.8170.0671567.4
Phi(~Sex + Age + Age2)p(~Sex + time)442009.84.2070.0551570.1
Phi(~Sex)p(~Sex + time)422011.76.1130.0211576.7
Phi(~Sex * Age_class + Age)p(~Sex + time)472012.46.8210.0151565.7
Age_class: age class at capture (teneral, immature, and mature); Age: number of days since the first capture. The best parsimonious model is highlighted in bold.
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Youcefi, A.; Mahdjoub, H.; Zebsa, R.; Kahalerras, A.; Amari, H.; Zouaimia, A.; Bensouilah, S.; Khelifa, R. The Effect of Age on Survival Is Similar in Males and Females of an Aquatic Insect Species. Ecologies 2024, 5, 491-501. https://doi.org/10.3390/ecologies5030030

AMA Style

Youcefi A, Mahdjoub H, Zebsa R, Kahalerras A, Amari H, Zouaimia A, Bensouilah S, Khelifa R. The Effect of Age on Survival Is Similar in Males and Females of an Aquatic Insect Species. Ecologies. 2024; 5(3):491-501. https://doi.org/10.3390/ecologies5030030

Chicago/Turabian Style

Youcefi, Abdeldjalil, Hayat Mahdjoub, Rabah Zebsa, Amin Kahalerras, Hichem Amari, Abdelheq Zouaimia, Soufyane Bensouilah, and Rassim Khelifa. 2024. "The Effect of Age on Survival Is Similar in Males and Females of an Aquatic Insect Species" Ecologies 5, no. 3: 491-501. https://doi.org/10.3390/ecologies5030030

APA Style

Youcefi, A., Mahdjoub, H., Zebsa, R., Kahalerras, A., Amari, H., Zouaimia, A., Bensouilah, S., & Khelifa, R. (2024). The Effect of Age on Survival Is Similar in Males and Females of an Aquatic Insect Species. Ecologies, 5(3), 491-501. https://doi.org/10.3390/ecologies5030030

Article Metrics

Back to TopTop