Skip to main content
Log in

Ecophysiological responses of the desert isopod Hemilepistus reaumurii to the combined effects of thermoperiod and photoperiod

  • Original Article
  • Published:
Biologia Aims and scope Submit manuscript

Abstract

Life in desert ecosystems forces animals to adopt adaptive strategies to cope with severe environmental conditions. Their ability to colonize these bioclimatic stages makes Hemilepistus reaumurii, a xeric terrestrial isopod, a very interesting model where the different strategies of its life history can be studied. In the present work, we aim to emphasize the inflexibility and the dependence of the reproductive features of this xeric species to day length and temperature type (periodic or constant). Their ability to change the timing of the breeding onset and adjust their life-history traits according to the stimulating experimental conditions to better succeed during the breeding period and therefore their survival, and to succeed in the colonization of severe bioclimatic stages are also highlighted. To do so, six photoperiodic regimes were combined with two different thermophase and cryophase (durations of 25:15 °C. Two additional conditions were tested where females were maintained under both aperiodic regimes and a constant temperature of 20 °C. Our results suggest that under constant temperature, the lag time is significantly shorter in females maintained under continuous light compared to those kept in the dark. In addition, we noted that between delaying the breeding and breeding earlier, the response shown by the animals varied significantly between the shorter and longer photophases when combined with the thermoperiodic regime. However, only the females that had been reared under breeding conditions with longer photophases, from 12 to 24 h, were observed to successfully release their manca.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Achouri MS (2012) Breeding phenology and reproductive strategies in terrestrial isopod species (Crustacea Isopoda Oniscidea) from Tunisia. In: Zhang X (ed) Phenology and climate change. InTech, China, pp 21–34. https://doi.org/10.5772/36234

  • Araujo PB, Bond-Buckup G (2005) Population structure and reproductive biology of Atlantoscia floridana (van Name, 1940) (Crustacea, Isopoda, Oniscidea) in southern Brazil. Acta Oecol 28:289–298. https://doi.org/10.1016/j.actao.2005.05.005

  • Ayari A, Raimond M, Souty-Grosset C, Nasri-Ammar K (2016a) Hierarchical organization of the cuticle of the subsocial desert isopod, Hemilepistus reaumurii. J Struct Biol 193:115–123. https://doi.org/10.1016/j.jsb.2015.12.005

    Article  PubMed  Google Scholar 

  • Ayari A, Richard FJ, Souty-Grosset C, Nasri-Ammar K (2016b) Family identity of the sub-social desert terrestrial isopod Hemilepistus reaumurii. J Arid Environ 134:10–16. https://doi.org/10.1016/j.jaridenv.2016.06.012

    Article  Google Scholar 

  • Ayari A (2018) Strategies de survie de l’Oniscoïde semi-désertique Hemilepistus reaumurii en Tunisie. Thèse Université de Tunis, 267 pp

  • Ayari A, Touihri M, Ghemari C, Nasri-Ammar K (2018) Hourly and monthly variations in the surface activity patterns of Hemilepistus reaumurii in arid environments of Tunisia. J Arid Land. https://doi.org/10.1007/s40333-018-0058-2

    Article  Google Scholar 

  • Beck SD (1983) Insect thermoperiodism. Rev Ent 28:91–108

    Article  Google Scholar 

  • Beck SD (1985) Effects of thermoperiod on photoperiodic determination of larval diapause in Ostrinia nubilalis. J Insect Physiol 31:41–46

    Article  Google Scholar 

  • Beck SD (1987) Thermoperiod-photoperiod interactions in the determination of diapause in Ostrinia nubilalis. J Insect Physiol 33:707–712

    Article  Google Scholar 

  • Chentoufi A (1988) Etude de la régulation photopériodique chez le Crustacé Isopode terrestre Armadillidium vulgare Latreille: Analyse expérimentale de la mesure du temps photopériodique. Thèse d’Etat, Université de Poitiers, 118 pp

  • Danks HV (1987) Insect dormancy: An ecological perspective. Biological survey of Canada (terrestrial arthropods). Ottawa, Biological Survey of Canada Monograph Series No. 1, 439 pp

  • Edney EB (1954) Woodlice and the land habitat. Biol Rev 29:185–219

    Article  Google Scholar 

  • Edney EB (1968) Transition from water to land in isopod crustaceans. Am Zool 8:309–326

    Article  Google Scholar 

  • Ghemari C, Ayari A, Khemaissia H, Nasri-Ammar K (2017) Photoperiod and male-presence effects on the onset of reproduction of Porcellio laevis (Oniscidea). Biologia 72:1480–1485. https://doi.org/10.1515/biolog-2017-0168

    Article  Google Scholar 

  • Gongalsky KB, Savin FA, Pokarzhevskii AD, Filimonova ZV (2005) Spatial distribution of isopods in an oak-beech forest. Eur J Soil Biol 41:117–122. https://doi.org/10.1016/j.ejsobi.2005.09.012

    Article  Google Scholar 

  • Hayder F (2016) Caractérisation du cycle de vie d’Hemilepistus reaumurii dans la région de Gabes. Mastère Université de Tunis, 63 pp

  • Hoffman G (1983) The search behavior of the desert isopod Hemilepistus reaumuri as compared with a systematic search. Behav Ecol Sociobiol 13:93–106

  • Hornung E, Warburg MR (1993) Breeding patterns in the oniscid isopod, Porcellio ficulneus Verh., at high temperature and under different photophases. Invertebr Reprod Dev 23:151–158. https://doi.org/10.1080/07924259.1993.9672306

    Article  Google Scholar 

  • Hornung E (2011) Evolutionary adaptation of oniscidean isopods to terrestrial life: structure, physiology and behavior. Terr Arthropod Rev 4:95–130

    Article  Google Scholar 

  • Juchault P, Mocquard JP, Bougrier N, Besse G (1980) Croissance et cycle reproducteur du Crustacé Isopode Oniscoïde Eluma purpurascens Budde-Lund. Etude dans la nature et au laboratoire, sous différentes conditions de température et de photopériode, d’une population du centre-ouest de la France. Vie Milieu 30:140–156

    Google Scholar 

  • Kacem H, Rezig M (1995) Cycle biologique d’Hemilepistus reaumuri (Audouin et Savigny, 1826) (Crustace, Isopode, Oniscoϊde). Bull Soc Sci Nat Tunis 24:56–65

    Google Scholar 

  • Kashani GM, Sari A, Hosseinie S, Malek M, Entezari E (2011) Life cycle and population structure of the terrestrial isopod Hemilepistus klugii (Brandt, 1833) (Isopoda: Oniscidea) in Iran. J Nat Hist 45:2081–2094. https://doi.org/10.1080/00222933.2011.582965

    Article  Google Scholar 

  • Lavelle P (1996) Diversity of soil fauna and ecosystem function. Biol Int 33:3–16

    Google Scholar 

  • Lavelle P, Decaens T, Aubert M, Barot S, Blouin M, Bureau F, Margerie P, Mora P, Rossi JP (2006) Soil invertebrates and ecosystem services. Eur J Soil Biol 42:315. https://doi.org/10.1016/j.ejsobi.2006.10.002

    Article  Google Scholar 

  • Linsenmair KE (1974) Some adaptations of the desert woodlouse Hemilepistus reaumuri (Isopoda, Oniscoidea) to desert environment. Verh Ges Okol 4:183–185

    Google Scholar 

  • Linsenmair KE (1984) Comparative studies on the social behaviour of the desert isopod Hemilepistus reaumuri and of a Porcellio species. In: Sutton SL, Holdich DM (eds) The biology of terrestrial isopods. Clarendon Press, Oxford, pp 423–454

    Google Scholar 

  • Linsenmair KE (1985) Individual and family recognition in subsocial arthropods, in particular, in the desert isopod Hemilepistus reaumuri. Fortschr Zool 31:411–434

    Google Scholar 

  • Linsenmair KE (1989) Sex-specific reproductive patterns in some terrestrial isopods. In: Rasa AE, Vogel C, Voland E (eds) The sociobiology of sexual and reproductive strategies. Chapman & Hall, London, pp 19–47

    Google Scholar 

  • Linsenmair KE (2007) Sociobiology of terrestrial isopods. In: Duffy JE, Thiel M (eds) Evolutionary ecology of social and sexual systems: crustaceans as model organisms. Oxford University Press, New York, pp 339–364

    Chapter  Google Scholar 

  • Longcore T (2003) Terrestrial arthropods as indicators of ecological restoration success in Coastal Sage Scrub (California, U.S.A). Restor Ecol 11:397–409. https://doi.org/10.1046/j.1526-100X.2003.rec0221.x

    Article  Google Scholar 

  • McQueen DJ, Steel CGH (1980) The role of photoperiod and temperature in the initiation of reproduction in the terrestrial isopod Oniscus asellus Linnaeus. Can J Zool 58:235–240. https://doi.org/10.1139/z80-027

    Article  Google Scholar 

  • Medini-Bouaziz L, El Gtari M, Hamaied S, Charfi-Cheikhrouha F (2017a) Population dynamics and reproductive aspects of Porcellio albinus (Isopoda, Oniscidea) of Zarat (Gabes, Tunisia). Invertebr Reprod Dev 61:18–26. https://doi.org/10.1080/07924259.2016.1263242

    Article  Google Scholar 

  • Medini-bouaziz L, Naceur-Fessi A, Charfi-Cheikhrouha F (2017b) Breeding patterns in the pre-desert oniscid isopod Porcellio buddelundi of Matmata (Gabès, Tunisia). Invertebr Reprod Dev 61:218–224. https://doi.org/10.1080/07924259.2017.1331936

    Article  Google Scholar 

  • Medini-Bouaziz L (2018) Behavioral and reproductive strategies of Porcellio species (Oniscidea) in Tunisian pre-desert ecosystems. IntechOpen. https://doi.org/10.5772/intechopen.76191

  • Mocquard JP, Juchault P, Souty-Grosset C (1989) The role of environmental factors (temperature and photoperiod) in the reproduction of the terrestrial isopod Armadillidium vulgare (Latreille, 1804). Monit Zool Ita Monogr 4:455–475

    Google Scholar 

  • Musolin D, Tsytsulina K, Itoa K (2004) Photoperiodic and temperature control of reproductive diapause induction in the predatory bug Orius strigicollis (Heteroptera: Anthocoridae) and its implications for biological control. Biol Control 31:91–98. https://doi.org/10.1016/j.biocontrol.2004.04.001

    Article  Google Scholar 

  • Nasri K (1993) Cycles saisonniers de la reproduction chez les Crustacés Isopodes terrestres: Etude expérimentale des modalités de la réponse photopériodique chez Hemilepistus reaumuri (Audouin et Savigny) et Armadillidium vulgare Latreille. Thèse de doctorat, Université de Poitiers

  • Nasri K, Juchault P, Mocquard JP, Souty-Grosset C (1996) Reproduction saisonnière chez Hemilepistus reaumuri (Audouin & Savigny, 1826), isopode terrestre des zones semi-arides. Crustaceana 69:223–235

  • Nasri-Ammar K, Morgan E (2005) Preliminary observations on the natural variation in the endogenous rhythm of the desert isopod Hemilepistus reaumurii. Eur J Soil Biol 41:63–68. https://doi.org/10.1016/j.ejsobi.2005.09.005

    Article  Google Scholar 

  • Nasri-Ammar K, Jelassi R, Ayari A, Morgan E (2016) Seasonal changes of locomotor activity patterns in the desert isopod Hemilepistus reaumuri. Biol Rhythm Res 47:25–38. https://doi.org/10.1080/09291016.2015.1073458

    Article  Google Scholar 

  • Oliver PG, Meechan CJ (1993) Woodlice. Synopses of the British fauna 49. Field Studies Council, Shrewsbury

  • Paoletti MG, Hassall M (1999) Woodlice (Isopoda: Oniscidea): Their potential for assessing sustainability and use as bioindicators. Agric Ecosyst Environ 74:157–165. https://doi.org/10.1016/S0167-8809(99)00035-3

    Article  Google Scholar 

  • Powers LW, Bliss DE (1983) Terrestrial adaptations. In: Vernberg FJ, Vernberg WB (eds) The biology of Crustacea: environmental adaptations. Academic Press, New York, pp 272–333

  • Quadros AF, Araujo PB (2008) An assemblage of terrestrial isopods (Crustacea) in southern Brazil and their contribution to leaf litter processing. Rev Bras Zool 25:58–66

    Article  Google Scholar 

  • Saulich AK, Volkovich TA, Goryshin NI (1983) Photoperiodic control of development of Loxostege sticticalis in nature. Zool Zh 62:1663–1675

    Google Scholar 

  • Saunders DS (2014) Insect photoperiodism: effects of temperature on the induction of insect diapause and diverse roles for the circadian system in the photoperiodic response. Entomol Sci 17:25–40. https://doi.org/10.1111/ens.12059

    Article  Google Scholar 

  • Schildknecht H, Eßwein U, Hering W, Blaschke C, Linsenmair KE (1988) Pheromone discrimination in the social desert arthropod Hemilepistus reaumuri. Z Naturforsch 43:613–620

    Article  CAS  Google Scholar 

  • Shachak M (1980) Energy allocation and life history strategy of the desert isopod Hemilepistus reaumuri. Oecologia 45:404–413

    Article  Google Scholar 

  • Shachak M, Yair A (1984) Population dynamics and the role of Hemilepistus reaumuri in a desert ecosystem. In: Sutton SL, Holdich DM (eds) The biology of terrestrial isopods. Symposium of the Zoological Society of London 53, Oxford Science Publications, pp 295–314

  • Sibly RM (1995) Life-history evolution in spatially heterogeneous environments, with and without phenotypic plasticity. Evol Ecol 9:242–257

    Article  Google Scholar 

  • Souty-Grosset C, Chentoufi A, Mocquard JP, Juchault P (1988) Seasonal reproduction in the terrestrial isopod Armadillidium vulgare (Latreille): geographical variability and genetic control of the response to photoperiod and temperature. Invert Reprod Dev 14:131–151. https://doi.org/10.1080/01688170.1988.10510373

    Article  Google Scholar 

  • Souty-Grosset C, Chentoufi A, Juchault P, Mocquard JP (1991) Combined effects of thermoperiod and photoperiod on the reproduction of a terrestrial isopod Armadillidium vulgare (Latreille): Geographical variability. J Therm Biol 16:233–240. https://doi.org/10.1016/0306-4565(91)90031-V

  • Warburg MR (1965) The microclimate in the habitats of two isopod species in southern Arizona. Am Midl Nat 73:363–375

    Article  Google Scholar 

  • Warburg M (1968) Behavioral adaptations of terrestrial isopods. Am Zool 8:545–561

    Article  Google Scholar 

  • Warburg MR (1987) Isopods and their terrestrial environment. Adv Ecol Res 17:187–242

    Article  Google Scholar 

  • Warburg MR (1992) Reproductive patterns in three isopod species from the Negev Desert. J Arid Environ 22:73–85

    Article  Google Scholar 

  • Warburg MR (1994) Review of recent studies on reproduction in terrestrial isopods. Invert Reprod Dev 26:45–62

    Article  Google Scholar 

  • Warburg MR (1995) Continuous breeding in two rare, fossorial, oniscid isopod species from the Central Negev Desert. J Arid Environ 29:383–393

    Article  Google Scholar 

  • Warburg MR (2011) Cost of breeding in oniscid isopods: a partial review. Crustaceana 84:1561–1580

    Article  Google Scholar 

  • Willows R (1984) Breeding phenology of woodlice and oostegite development in Ligia oceanica (L.) (Crustacea). Symp Zool Soc Lond 53:469–485

    Google Scholar 

  • Wu S, Refinetti R, Kok LT, Youngman RR, Reddy GVP, Xue F (2014) Photoperiod and temperature effects on the adult eclosion and mating rhythms in Pseudopidorus fasciata (Lepidoptera: Zygaenidae). Environ Entomol 43:1650–1655. https://doi.org/10.1603/EN14164

    Article  PubMed  Google Scholar 

  • Zimmer M, Kautz G, Topp W (2003) Leaf litter-colonizing microbiota: supplementary food source or indicator of food quality for Porcellio scaber (Isopoda: Oniscidea). Eur J Soil Biol 39:209–216. https://doi.org/10.1016/j.ejsobi.2003.07.001

    Article  Google Scholar 

Download references

Acknowledgements

The present study was supported by the Laboratory of Diversity, Management and Conservation of Biological Systems (LR18ES06), University of Tunis El Manar, Faculty of Science of Tunis. We wish to thank Mrs. Najwa Abdelkefi MSci. Astrophysics Translator/Interpreter for his constructive remarks and for revising the English of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Amal Habassi.

Ethics declarations

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Conflict of interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Habassi, A., Khemaissia, H. & Nasri-Ammar, K. Ecophysiological responses of the desert isopod Hemilepistus reaumurii to the combined effects of thermoperiod and photoperiod. Biologia 75, 2251–2260 (2020). https://doi.org/10.2478/s11756-020-00480-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.2478/s11756-020-00480-4

Keywords

Navigation