Egg morphology may underpin the successful distribution of large branchiopods in temporary waters

Abstract

Invertebrate species from temporary aquatic ecosystems produce resistant dormant stages (i.e. eggs) that accumulate in long lived mixed egg banks in the sediment. These dormant eggs not only bridge dry phases but also act as propagules for passive dispersal. Large branchiopod crustaceans (e.g. Notostraca, Anostraca and Spinicaudata) produce dormant eggs of variable shapes, sizes and external ornamentation. While these characteristics are often species-specific and have been used in taxonomy, little is known about their ecological significance, for example, their contribution to colonisation success. Here, we explore the idea that variation in egg morphology may impact vector-mediated dispersal and colonisation success of large branchiopods. We studied egg banks from 98 temporary waters across the Northern Cape, South Africa and assessed whether distribution and densities of eggs carried a morphological signal. Overall, our results imply that both size and external structures may impact dispersal to and successful colonisation of temporary waters by large branchiopods. Specifically, our results show that small propagules (< 200 µm) and eggs with external traits (hooks or spines) that facilitate substrate adhesion were most confined in their distribution. In contrast, large (> 400 µm), smooth eggs and medium sized (200–300 µm), polygonal eggs were most widely distributed. Ultimately, our approach provides insight in actual colonisation success of species with different egg types and not only on the propensity of the eggs to be picked up and transported by vectors.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Availability of data and material

The data support our published claims and comply with field standards. All raw data used in this study belongs to SAEON. Please contact the corresponding author for data sharing options.

Code availability

Not applicable. Standard statistical analyses were applied using the software package PAST 4.0.

References

  1. Ali AJ, Dumont HJ (1995) Larviculture of the fairy shrimp, Streptocephalus proboscideus (Crustacea: Anostraca): effect of food concentration and physical and chemical properties of the culture medium. Hydrobiologia 298:159–165

    CAS  Article  Google Scholar 

  2. Andersen MC (1993) Diaspore Morphology and Seed Dispersal in Several Wind-Dispersed Asteraceae. Am J Bot 80:487–492

    PubMed  Article  Google Scholar 

  3. Anderson MD (2000) The status of flamingos in the Northern Cape Province. South Africa Ostrich 71:425–437

    Google Scholar 

  4. Belmonte G, Miglietta A, Rubino F, Boero F (1997) Morphological convergence of resting stages of planktonic organisms: a review. Hydrobiologia 355:159–165

    Article  Google Scholar 

  5. Bernatowicz P, Radzikowski J, Paterczyk B, Bebas P, Slusarczyk M (2018) Internal structure of Daphnia ephippium as an adaptation to dispersion. Zoologischer Anzeiger 277:12–22

    Article  Google Scholar 

  6. Bilton DT, Freeland JR, Okamura B (2001) Dispersal in freshwater invertebrates. Annu Rev Ecol Syst 32:159–181

    Article  Google Scholar 

  7. Bohonak AJ, Jenkins DG (2003) Ecological and evolutionary significance of dispersal by freshwater invertebrates. Ecol Lett 6:783–796

    Article  Google Scholar 

  8. Boven L, Vanschoenwinkel B, De Roeck E, Hulsmans A, Brendonck L (2008) Diversity and distribution of large branchiopods in Kiskunság (Hungary) in relation to local habitat and spatial factors: implications for their conservation. Mar Freshw Res 59:940–950

    Article  Google Scholar 

  9. Brendonck L (1996) Diapause, quiescence, hatching requirements: what we can learn from large freshwater branchiopods (Crustacea: Branchiopoda: Anostraca, Notostraca, Conchostraca). Hydrobiologia 320:85–97

    Article  Google Scholar 

  10. Brendonck L, Coomans A (1994a) Egg morphology in African Streptocephalidae (Crustacea: Branchiopoda: Anostraca) Part 1: South of Zambezi and Kunene rivers Archiv für Hydrobiologie/Suppl 99 (Monographische Beiträge) 3:313-334

  11. Brendonck L, Coomans A (1994b) Egg morphology in African Streptocephalidae (Crustacea: Branchiopoda: Anostraca). Part 2: North of Zambezi and Kunene rivers, and Madagascar Archiv für Hydrobiologie/Suppl 99 (Monographische Beiträge) 3:335-356

  12. Brendonck L, de Meester L (2003) Egg banks in freshwater zooplankton: evolutionary and ecological archives in the sediment. Hydrobiologia 491:65–84

    Article  Google Scholar 

  13. Brendonck L, Riddoch BJ (1997) Anostracans (Branchiopoda) of Botswana: morphology, distribution, diversity, and endemicity. J Crustac Biol 17:111–134

    Article  Google Scholar 

  14. Brendonck L, Riddoch BJ (2000) Dispersal in the desert rock pool anostracan Branchipodopsis wolfi (Brancliiopoda: Anostraca). Biodiversity Crisis Crustacea 12:109–118

    Google Scholar 

  15. Brendonck L, Thiéry A, Coomans A (1990) Taxonomy and biogeography of the Galapagos branchiopod fauna (Anostraca, Notostraca, Spinicaudata). J Crustac Biol 10:676–694

    Article  Google Scholar 

  16. Brendonck L, Hamer M, Thiéry A (1992) Occurrence of tetrahedral eggs in the Streptocephalidae Daday (Branchiopoda: Anostraca) with descriptions of a new subgenus, Parastreptocephalus, and a new species, Streptocephalus (Parastreptocephalus) zuluensis Brendonck and Hamer. J Crustac Biol 12:282–297

    Article  Google Scholar 

  17. Brendonck L, Rogers DC, Olesen J, Weeks S, Hoeh WR (2008) Global diversity of large branchiopods (Crustacea: Branchiopoda) in freshwater. Hydrobiologia 595:167–176

    Article  Google Scholar 

  18. Brendonck L, Pinceel T, Ortells R (2016) Dormancy and dispersal as mediators of zooplankton population and community dynamics along a hydrological disturbance gradient in inland temporary pools. Hydrobiologia 796:201–222

    Article  CAS  Google Scholar 

  19. Brochet AL, Gauthier-Clerc M, Guillemain M, Fritz H, Waterkeyn A, Green AJ (2010) Field evidence of dispersal of branchiopods, ostracods and bryozoans by teal (Anas crecca) in the Camargue (southern France). Hydrobiologia 637:255–261

    Article  Google Scholar 

  20. Cáceres CE, Soluk DA (2002) Blowing in the wind: a field test of overland dispersal and colonization by aquatic invertebrates. Oecologia 131:402–408

    PubMed  Article  Google Scholar 

  21. Charalambidou I, Ketelaars HAM, Santamaria L (2003) Endozoochory by ducks: influence of developmental stage of Bythotrephes diapause eggs on dispersal probability. Divers Distrib 9:367–374

    Article  Google Scholar 

  22. Crossland (1965) The Pest Status and Control of the Tadpole Shrimp, Triops granarius, and of the Snail, Lanistes ovum, in Swaziland Rice Fields. J Appl Ecol 2:115–120

    Article  Google Scholar 

  23. Czyż MJ, Woliński P, Goldyn B (2016) Cyst morphology of large branchiopod crustaceans (Anostraca, Notostraca, Laevicaudata, Spinicaudata) in western. Poland Biol Lett 53:79–88

    Article  Google Scholar 

  24. De Roeck E, Vanschoenwinkel B, Day J, Xu Y, Raitt L, Brendonck L (2007) Conservation status of large branchiopods in the Western Cape, South Africa. Wetlands 27:162–173

    Article  Google Scholar 

  25. De Roeck E, Waterkeyn A, Brendonck L (2010) Life-history traits of Streptocephalus purcelli Sars, 1898 (Branchiopoda, Anostraca) from temporary waters with different phenology. Water SA 36:323–328

    Google Scholar 

  26. Dumont HJ, Nandini S, Sarma SSS (2002) Cyst ornamentation in aquatic invertebrates: a defence against egg-predation. Hydrobiologia 486:161–167

    Article  Google Scholar 

  27. Dzialowski AR, O’Brien WJ, Swaffar SM (2000) Range expansion and potential dispersal mechanisms of the exotic cladoceran Daphnia lumholtzi. J Plankton Res 22:2205–2223

    Article  Google Scholar 

  28. Figuerola J, Green AJ (2002) Dispersal of aquatic organisms by waterbirds: a review of past research and priorities for future studies. Freshw Biol 47:483–494

    Article  Google Scholar 

  29. Fryer G (1996) Diapause, a potent force in the evolution of freshwater crustaceans. Hydrobiologia 320:1–14

    Article  Google Scholar 

  30. Graham TB, Wirth D (2008) Dispersal of large branchiopod cysts: potential movement by wind from potholes on the Colorado Plateau. Hydrobiologia 600:17–27

    Article  Google Scholar 

  31. Green AJ, Figuerola J (2005) Recent advances in the study of long-distance dispersal of aquatic invertebrates via birds. Divers Distrib 11:149–156

    Article  Google Scholar 

  32. Green AJ, Figuerola J (2007) High dispersal capacity of a broad spectrum of aquatic invertebrates via waterbirds. Aquat Sci 69:568–574

    Article  Google Scholar 

  33. Green AJ, Jenkins KM, Bell D, Morris PJ, Kingsford RT (2008) The potential role of waterbirds in dispersing invertebrates and plants in arid Australia. Freshw Biol 53:380–392

    Google Scholar 

  34. Griesser M, Halvarsson P, Sahlman T, Ekman J (2014) What are the strengths and limitations of direct and indirect assessment of dispersal? Insights from a long-term field study in a group-living bird species. Behav Ecol Sociobiol 68:485–497

    Article  Google Scholar 

  35. Hairston NG, Cáceres CE (1996) Distribution of crustacean diapause: micro- and macroevolutionary pattern and process. Hydrobiologia 320:27–44

    Article  Google Scholar 

  36. Hammer Ø, Harper DAT, Ryan PD (2001) PAST: Paleontological Statistical software package for education and data analysis vol 4, 1 edn. Palaeontologia Electronica,

  37. Herremans M (1999) Waterbird diversity, density, communities and seasonality in the Kalahari Basin, Botswana. J Arid Environ 43:319–350

    Article  Google Scholar 

  38. Herrmann E, Anderson MD, Seaman MT (2004) Occurrence and abundance of waterbirds at an ephemeral pan in the Northern Cape Province. South Africa Ostrich 75:275–284

    Article  Google Scholar 

  39. Hill RE, Shepard WD (1997) Observations on the identification of California anostracan cysts. Hydrobiologia 359:113–123

    Article  Google Scholar 

  40. Incagnone G, Marrone F, Barone R, Robba L, Naselli-Flores L (2015) How do freshwater organisms cross the ‘‘dry ocean’’? A review on passive dispersal and colonization processes with a special focus on temporary ponds. Hydrobiologia 750:103–123

    Article  Google Scholar 

  41. Kraus H, Eder E, Møller OS, Werding B (2004) Cyst deposition behaviour and the functional morphology of the brood pouch in Streptocephalus torvicornis (Branchiopoda: Anostraca). J Crustac Biol 24:393–397

    Article  Google Scholar 

  42. Louette G, De Meester L (2005) High dispersal capacity of cladoceran zooplankton in newly founded communities. Ecology 86:353–359

    Article  Google Scholar 

  43. Macdonald KS, Sallenave R, Cowley DE (2011) Morphologic and genetic variation in Triops (Branchiopoda: Notostraca) From ephemeral waters of the Northern Chihuahuan Desert of North America. J Crustac Biol 31:468–484

    Article  Google Scholar 

  44. Machado M, Guilherme L, da Fonesca LC, Galioto ED, Caramujo MJ (2017) First record of the tadpole shrimp Triops cancriformis (Lamarck 1801 (Crustacea: Branchiopoda: Notostraca) in Portugal. Limnetica 36:543–555

    Google Scholar 

  45. Maffei C, Mura G, Zarattini P (2002) Assessing anostracan (Crustacea: Branchiopoda) cyst bank size: An attempt at a standardized method. Hydrobiologia 486:255–261

    Article  Google Scholar 

  46. Marcus NH (1990) Calanoid copepod, cladoceran, and rotifer eggs in sea bottom sediments of northern Californian coastal waters: identification, occurrence and hatching Marine Biology 105

  47. Martin JW (1992) Branchiopoda. In: Harrison FW (ed) Microscopic Anatomy of Invertebrates, vol 9. Wiley-Liss, New York, pp 25–224

    Google Scholar 

  48. Meyer-Milne E, Mlambo MC (2019) A tale of records from Hakskeen Pan, the first record of Pumilibranchipus deserti Hamer and Brendonck, 1995 (Anostraca, Branchiopoda) from South Africa and the pursuit of a new world land speed record. African J Aquatic Sci 44:409–413

    Article  Google Scholar 

  49. Mura G (1991) Sem Morphology of Resting Eggs in the Species of the Genus Branchinecta from North America. J Crustac Biol 11:432–436

    Article  Google Scholar 

  50. Mura G (1992) Additional remarks on cyst morphometrics in Anostracans and its significance. Part II: Egg morphology. Crustaceana 63:225–246

    Article  Google Scholar 

  51. Mura G (2001) Morphological diversity of the resting eggs in the anostracan genus Chirocephalus (Crustacea, Branchiopoda). Hydrobiologia 450:173–185

    Article  Google Scholar 

  52. Mura G (2004) Structure and Functioning of the “Egg Bank” of a Fairy Shrimp in a Temporary Pool: chirocephalus ruffoi from Pollino National Park (Southern Italy) as a Case Study. Int Rev Hydrobiol 89:35–50

    Article  Google Scholar 

  53. Mura G, Thiéry A (1986) Taxonomical significance of scanning electron microscopic morphology of the Euphyllopods’ resting eggs from Morocco. Part I. Anostraca Vie Milieu 36:125–131

    Google Scholar 

  54. Nathan R, Schurr FM, Spiegel O, Steinitz O, Trakhtenbrot A, Tsoar A (2008) Mechanisms of long-distance seed dispersal. Trends Ecol Evol 23:638–647

    PubMed  Article  Google Scholar 

  55. Nock CA, Vogt RJ, Beisner BE (2016) Functional Traits. In: eLS: Ecology. John Wiley & Sons Ltd, Chichester

  56. Onbé T (1978) Sugar flotation method for sorting the resting eggs of marine cladocerans and copepods from sea-bottom sediments of Ise Bay and Uragami Inlet. Central Jpn Bull Jpn Soc Sci Fisher 44:1411

    Article  Google Scholar 

  57. Padhye S, Dahanukar N (2015) Distribution and assemblages of large branchiopods (Crustacea: Branchiopoda) of northern Western Ghats, India. J Limnol 74:371–380

    Google Scholar 

  58. Padhye S, Timms BV, Ghate HV (2016) Large branchiopod (Crustacea: Branchiopoda) egg morphology of Western Ghats, Maharashtra, India. Zootaxa 4079:246–254

    PubMed  Article  Google Scholar 

  59. Parekh PA, Paetkau MJ, Gosselin LA (2014) Historical frequency of wind dispersal events and role of topography in the dispersal of anostracan cysts in a semi-arid environment. Hydrobiologia 740:51–59

    Article  Google Scholar 

  60. Pietrzak B, Ślusarczyk M (2006) The fate of the ephippia - Daphnia dispersal in time and space. Polish J Ecol 54:709–714

    Google Scholar 

  61. Pinceel T, Vanschoenwinkel B, Brendonck L (2013) Flexible dispersal dimorphism in zooplankton resting eggs: an example of repeated phenotypic coin flipping? Biol J Lin Soc 110:749–756

    Article  Google Scholar 

  62. Pinceel T, Brendonck L, Vanschoenwinkel B (2015) Propagule size and shape may promote local wind dispersal in freshwater zooplankton—a wind tunnel experiment. Limnol Oceanogr 61:122–131

    Article  Google Scholar 

  63. Pinceel T, Vanschoenwinkel B, Brendonck L, Buschke FT (2016) Modelling the sensitivity of life history traits to climate change in a temporary pool crustacean. Sci Rep 6:29451

    PubMed  PubMed Central  Article  Google Scholar 

  64. Rabet N (2010) Revision of the egg morphology of Eulimnadia (Crustacea, Branchiopoda, Spinicaudata). Zoosystema 32:373–391

    Article  Google Scholar 

  65. Reynolds C, Cumming GS (2015) The role of waterbirds in the dispersal of freshwater cladocera and bryozoa in southern Africa. African Zool 50:307–311

    Article  Google Scholar 

  66. Ripley BJ, Holtz J, Simovich MA (2004) Cyst bank life-history model for a fairy shrimp from ephemeral ponds. Freshw Biol 49:221–231

    Article  Google Scholar 

  67. Rivas J, Schröder T, Gill TE, Wallace RL, Walsh EJ (2019) Anemochory of diapausing stages of microinvertebrates in North American drylands. Freshw Biol 64:1303–1314

    PubMed  PubMed Central  Article  Google Scholar 

  68. Rogers DC (2014) Larger hatching fractions in avian dispersed anostracan eggs (Branchiopoda). J Crustac Biol 34:135–143

    Article  Google Scholar 

  69. Schernhammer T, Wessely J, Eder E, Straka U, Essl F (2020) Modelling the distribution of large branchiopods (Crustacea: Notostraca, Anostraca & Spinicaudata) for predicting occurrences in poorly sampled regions. Global Ecol Conser 23:e01083

    Article  Google Scholar 

  70. Schwentner M, Timms BV, Richter S (2012) Flying with the birds? Recent large-area dispersal of four Australian Limnadopsis species (Crustacea: Branchiopoda: Spinicaudata). Ecol Evolut 2:1605–1626

    Article  Google Scholar 

  71. Seaman MT, Kok DJ, von Schlichting BJ, Kruger AJ (1991) Natural growth and reproduction in Triops granarius (Lucas) (Crustacea: Notostraca) Hydrobiologia 212

  72. Simmons RE, Barnard P, Jamieson IG (1998) What precipitates influxes of wetland birds to ephemeral pans in arid landscapes? Observations from Namibia. Ostrich 70:145–148

    Article  Google Scholar 

  73. Ślusarczyk M, Grabowski T, Pietrzak B (2017) Quantification of floating ephippia in lakes: a step to a better understanding of high dispersal propensity of freshwater plankters. Hydrobiologia 798:61–72

    Article  Google Scholar 

  74. Sorensen AE (1986) Seed dispersal by adhesion. Annu Rev Ecol Syst 17:443–463

    Article  Google Scholar 

  75. Tackenberg O, Römermann C, Thompson K, Poschlod P (2006) What does diaspore morphology tell us about external animal dispersal? Evidence from standardized experiments measuring seed retention on animal-coats. Basic Appl Ecol 7:45–58

    Article  Google Scholar 

  76. Tesson SVM et al (2016) Integrating microorganism and macroorganism dispersal: modes, techniques and challenges with particular focus on co-dispersal. Écoscience 22:109–124

    Article  Google Scholar 

  77. Thiéry A (1997) Horizontal distribution and abundance of cysts of several large branchiopods in temporary pool and ditch sediments. Hydrobiologia 359:177–189

    Article  Google Scholar 

  78. Thiéry A, Gasc C (1991) Resting eggs of Anostraca, Notostraca and Spinicaudata (Crustacea, Branchiopoda) occurring in France: identification and taxonomical value. Hydrobiologia 212:245–259

    Article  Google Scholar 

  79. Timms BV (2001) A study of the Werewilka Inlet of the saline Lake Wyara, Australia - a harbour of biodiversity for a sea of simplicity. Hydrobiologia 466:245–254

    Article  Google Scholar 

  80. Timms BV (2016) A partial revision of the Australian Eulimnadia Packard, 1874 (Branchiopoda: Spinicaudata: Limnadiidae). Zootaxa 4066:351–389

    PubMed  Article  Google Scholar 

  81. Timms BV, Lindsay S (2011) Morphometrics of the resting eggs of the fairy shrimp Branchinella in Australia (Anostraca: Thamnocephalidae). Proc Linnean Soc NSW 133:53–70

    Google Scholar 

  82. Timms BV, Shepard WD, Hill RE (2004) Cyst Shell Morphology of the Fairy Shrimps (Crustacea: Anostraca) of Australia. Proc Linnean Soc NSW 125:73–95

    Google Scholar 

  83. van de Meutter F, Stoks R, de Meester L (2008) Size-selective dispersal of Daphnia resting eggs by backswimmers (Notonecta maculata). Biol Let 4:494–496

    Article  Google Scholar 

  84. Vanschoenwinkel B, Gielen S, Seaman MT, Brendonck L (2008a) Any way the wind blows - frequent wind dispersal drives species sorting in ephemeral aquatic communities. Oikos 117:125–134

    Article  Google Scholar 

  85. Vanschoenwinkel B, Gielen S, Vandewaerde H, Seaman MT, Brendonck L (2008b) Relative importance of different dispersal vectors for small aquatic invertebrates in a rock pool metacommunity. Ecography 31:567–577

    Article  Google Scholar 

  86. Vanschoenwinkel B, Pinceel T, Vanhove MPM, Denis C, Jocqué M, Timms BV, Brendonck L (2012) Toward a Global Phylogeny of the ‘‘Living Fossil’’ Crustacean Order of the Notostraca. PLoS ONE 7:e34998. https://doi.org/10.31371/journal.pone.0034998

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  87. Verni F, Rosati G (2011) Resting cysts: A survival strategy in Protozoa Ciliophora Italian. J Zool 78:134–145

    Google Scholar 

  88. Viana DS, Santamaria L, Figuerola J (2016) Migratory Birds as Global Dispersal Vectors. Trends Ecol Evol 31:763–775

    PubMed  Article  Google Scholar 

  89. Waterkeyn A, Grillas P, Anton-Pardo M, Vanschoenwinkel B, Brendonck L (2011) Can large branchiopods shape microcrustacean communities in Mediterranean temporary wetlands? Mar Freshw Res 62:46–53

    CAS  Article  Google Scholar 

  90. Yan-bin S, Di-ying H (2008) Extant clam shrimp egg morphology: taxonomy and comparison with other fossil branchiopod eggs. J Crustac Biol 28:352–360

    Article  Google Scholar 

Download references

Acknowledgements

Dr E Milne was enabled through a Postdoctoral Fellowship of a Professional Development Programme funded by the South African Department of Science and Technology and the National Research Foundation; as well as a KU Leuven GLOBAL MINDS: Short Term Research Stay Mobility Grant. Additional project funding was provided through an NRF FBIP Grant (No. 110451) and the South African Environmental Observation Network provided continuing project support. We thank Alexander Vrijdagh from the KU Leuven Institute of Botany and Microbiology who performed the SEM photography, as well as all the landowners for allowing this research to be conducted on their properties. Rainfall and wind data was provided by the South African Weather Service.

Funding

Dr E Milne was enabled through a Postdoctoral Fellowship of a Professional Development Programme funded by the South African Department of Science and Technology and the National Research Foundation; as well as a KU Leuven GLOBAL MINDS: Short Term Research Stay Mobility Grant. Additional project funding was provided through an NRF FBIP Grant (No. 110451).

Author information

Affiliations

Authors

Contributions

Conceptualisation: [EM-M, TP]; Methodology: [EM-M]; Formal analysis and investigation: [EM-M]; Writing-original draft preparation: [EM-M]; Writing-review and editing: [TP, LB]; Funding acquisition: [EM-M]; Resources: [EM-M, LB].

Corresponding author

Correspondence to Elizabeth Meyer-Milne.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Handling Editor: Tėlesphore Sime-Ngando

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Meyer-Milne, E., Brendonck, L. & Pinceel, T. Egg morphology may underpin the successful distribution of large branchiopods in temporary waters. Aquat Ecol 55, 237–251 (2021). https://doi.org/10.1007/s10452-020-09826-1

Download citation

Keywords

  • Temporary waterbodies
  • Dispersal vectors
  • Adaptations
  • Adhesion traits
  • Crustacea