Does drought limit resprouter recruitment in Erica? A test using seeder and resprouter seedlings of Erica coccinea
Jenny Leonard A , Adam G. West A * , Justin J. van Blerk A and Fernando Ojeda BA Department of Biological Sciences, University of Cape Town, Private Bag X3, Rondebosch 7701, Cape Town, South Africa.
B Departmento de Biologia – Instituto de Investigaciones Vitivinicolas y Agroalimentarias (IVAGRO), Universidad de Cadiz, Campus Rio San Pedro, Puerto Real E-11510, Spain.
Australian Journal of Botany 69(8) 554-564 https://doi.org/10.1071/BT21015
Submitted: 6 February 2021 Accepted: 8 July 2021 Published: 20 October 2021
© 2021 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
Context: It has been proposed that the distribution of resprouter and seeder Erica in the Cape Floristic Region (CFR) of South Africa is determined by drought rather than by fire frequency. Seedlings of Erica seeders are predicted to withstand the mild droughts of the southwest CFR better than those of Erica resprouters, which would account for the abundance of seeders in this region.
Aims: This study aimed to test this hypothesis using Erica coccinea (L.), which contains both a resprouter and a seeder form.
Methods: One-year-old seedlings of both forms were subjected to a progressively severe 50-day drought in the greenhouse.
Key results: Contrary to expectations, seeder seedlings had 67% higher mortality than resprouters during the initial phase of drought (30% vs 18% after 32 days). However, both forms were unable to survive as the drought progressed, resulting in 95% mortality by Day 50. There were limited differences between the forms in gas exchange and water potential, and no difference in root:shoot ratios. However, resprouters had significantly higher soluble carbohydrates than did seeders, which may have aided in delaying mortality.
Conclusions: Our results showed no evidence of resprouter seedlings being more vulnerable to mild drought than seeders in E. coccinea.
Implications: Our findings challenge the hypothesis that the distribution of this species can be explained by the vulnerability of resprouter seedlings to mild drought.
Keywords: Cape Floristic Region, carbon starvation, drought, experiment, fynbos, greenhouse, hydraulic failure, mortality, non-structural carbohydrates, recruitment, sprouting.
References
Adams HD, Guardiola-Claramonte M, Barron-Gafford GA, Villegas JC, Breshears DD, Zou CB, Troch PA, Huxman TE (2009) Temperature sensitivity of drought-induced tree mortality portends increased regional die-off under global-change-type drought. Proceedings of the National Academy of Sciences 106, 7063–7066.| Temperature sensitivity of drought-induced tree mortality portends increased regional die-off under global-change-type drought.Crossref | GoogleScholarGoogle Scholar |
Alcoverro T, Zimmerman RC, Kohrs DG, Alberte RS (1999) Resource allocation and sucrose mobilization in light-limited eelgrass Zostera marina. Marine Ecology Progress Series 187, 121–131.
| Resource allocation and sucrose mobilization in light-limited eelgrass Zostera marina.Crossref | GoogleScholarGoogle Scholar |
Altwegg R, De Klerk HM, Midgley GF (2015) Fire-mediated disruptive selection can explain the reseeder–resprouter dichotomy in Mediterranean-type vegetation. Oecologia 177, 367–377.
| Fire-mediated disruptive selection can explain the reseeder–resprouter dichotomy in Mediterranean-type vegetation.Crossref | GoogleScholarGoogle Scholar | 25348575PubMed |
Anderegg WRL, Berry JA, Smith DD, Sperry JS, Anderegg LDL, Field CB (2012) The roles of hydraulic and carbon stress in a widespread climate-induced forest die-off. Proceedings of the National Academy of Sciences 109, 233–237.
| The roles of hydraulic and carbon stress in a widespread climate-induced forest die-off.Crossref | GoogleScholarGoogle Scholar |
Bell TL, Ojeda F (1999) Underground starch storage in Erica species of the Cape Floristic Region – differences between seeders and resprouters. New Phytologist 144, 143–152.
| Underground starch storage in Erica species of the Cape Floristic Region – differences between seeders and resprouters.Crossref | GoogleScholarGoogle Scholar |
Bellingham PJ, Sparrow AD (2000) Resprouting as a life history strategy in woody plant communities. Oikos 89, 409–416.
| Resprouting as a life history strategy in woody plant communities.Crossref | GoogleScholarGoogle Scholar |
Breshears DD, Myers OB, Meyer CW, Barnes FJ, Zou CB, Allen CD, McDowell NG, Pockman WT (2009) Tree die-off in response to global change-type drought: mortality insights from a decade of plant water potential measurements. Frontiers in Ecology and the Environment 7, 185–189.
| Tree die-off in response to global change-type drought: mortality insights from a decade of plant water potential measurements.Crossref | GoogleScholarGoogle Scholar |
Brodribb TJ, Cochard H (2009) Hydraulic failure defines the recovery and point of death in water-stressed conifers. Plant Physiology 149, 575–584.
| Hydraulic failure defines the recovery and point of death in water-stressed conifers.Crossref | GoogleScholarGoogle Scholar | 19011001PubMed |
Cowling RM, Ojeda F, Lamont BB, Rundel PW, Lechmere-Oertel R (2005) Rainfall reliability, a neglected factor in explaining convergence and divergence of plant traits in fire-prone mediterranean-climate ecosystems. Global Ecology and Biogeography 14, 509–519.
| Rainfall reliability, a neglected factor in explaining convergence and divergence of plant traits in fire-prone mediterranean-climate ecosystems.Crossref | GoogleScholarGoogle Scholar |
Cruz A, Pérez B, Velasco A, Moreno JM (2003) Variability in seed germination at the interpopulation, intrapopulation and intraindividual levels of the shrub Erica australis in response to fire-related cues. Plant Ecology 169, 93–103.
| Variability in seed germination at the interpopulation, intrapopulation and intraindividual levels of the shrub Erica australis in response to fire-related cues.Crossref | GoogleScholarGoogle Scholar |
da Costa ACL, Galbraith D, Almeida S, Portela BTT, da Costa M, de Athaydes Silva Junior J, Braga AP, de Gonçalves PHL, de Oliveira AAR, Fisher R, Phillips OL, Metcalfe DB, Levy P, Meir P (2010) Effect of 7 yr of experimental drought on vegetation dynamics and biomass storage of an eastern Amazonian rainforest. New Phytologist 187, 579–591.
| Effect of 7 yr of experimental drought on vegetation dynamics and biomass storage of an eastern Amazonian rainforest.Crossref | GoogleScholarGoogle Scholar |
Keeley JE, Zedler PH (1978) Reproduction of chaparral shrubs after fire: a comparison of sprouting and seeding strategies. American Midland Naturalist 99, 142–161.
| Reproduction of chaparral shrubs after fire: a comparison of sprouting and seeding strategies.Crossref | GoogleScholarGoogle Scholar |
Keeley JE, Bond WJ (1997) Convergent seed germination in South African fynbos and Californian chaparral. Plant Ecology 133, 153–167.
| Convergent seed germination in South African fynbos and Californian chaparral.Crossref | GoogleScholarGoogle Scholar |
Keeley JE, Pausas JG, Rundel PW, Bond WJ, Bradstock RA (2011) Fire as an evolutionary pressure shaping plant traits. Trends in Plant Science 16, 406–411.
| Fire as an evolutionary pressure shaping plant traits.Crossref | GoogleScholarGoogle Scholar | 21571573PubMed |
Kozlowski TT (1992) Carbohydrate sources and sinks in woody plants. The Botanical Review 58, 107–222.
| Carbohydrate sources and sinks in woody plants.Crossref | GoogleScholarGoogle Scholar |
Kraaij T, van Wilgen BW (2014) Drivers, ecology, and management of fire in fynbos. In ‘Fynbos: ecology, evolution, and conservation of a megadiverse region’. (Eds N Allsopp, JF Colville, GA Verboom) pp. 299–320. (Oxford University Press: Oxford, UK)
Le Maitre DC, Midgley JJ (1992) Plant reproductive ecology. In ‘The ecology of fynbos: nutrients, fire and diversity’. (Ed. RM Cowling) pp. 135–174. (Oxford University Press: Cape Town, South Africa)
Leonard J, West AG, Ojeda F (2018) Differences in germination response to smoke and temperature cues in ‘pyrophyte’ and ‘pyrofuge’ forms of Erica coccinea (Ericaceae). International Journal of Wildland Fire 27, 562–568.
| Differences in germination response to smoke and temperature cues in ‘pyrophyte’ and ‘pyrofuge’ forms of Erica coccinea (Ericaceae).Crossref | GoogleScholarGoogle Scholar |
Leuzinger S, Bigler C, Wolf A, Korner C (2009) Poor methodology for predicting large-scale tree die-off. Proceedings of the National Academy of Sciences 106, E106
| Poor methodology for predicting large-scale tree die-off.Crossref | GoogleScholarGoogle Scholar |
McDowell NG (2011) Mechanisms linking drought, hydraulics, carbon metabolism, and vegetation mortality. Plant Physiology 155, 1051–1059.
| Mechanisms linking drought, hydraulics, carbon metabolism, and vegetation mortality.Crossref | GoogleScholarGoogle Scholar | 21239620PubMed |
McDowell N, Pockman WT, Allen CD, Breshears DD, Cobb N, Kolb T, Plaut J, Sperry JS, West AG, Williams DG, Yepez EA (2008) Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? New Phytologist 178, 719–739.
| Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought?Crossref | GoogleScholarGoogle Scholar |
Mitchell PJ, O’Grady AP, Tissue DT, White DA, Ottenschlaeger ML, Pinkard EA (2013) Drought response strategies define the relative contributions of hydraulic dysfunction and carbohydrate depletion during tree mortality. New Phytologist 197, 862–872.
| Drought response strategies define the relative contributions of hydraulic dysfunction and carbohydrate depletion during tree mortality.Crossref | GoogleScholarGoogle Scholar |
Moreira B, Tormo J, Estrelles E, Pausas JG (2010) Disentangling the role of heat and smoke as germination cues in Mediterranean Basin flora. Annals of Botany 105, 627–635.
| Disentangling the role of heat and smoke as germination cues in Mediterranean Basin flora.Crossref | GoogleScholarGoogle Scholar | 20181568PubMed |
Moreira B, Tormo J, Pausas JG (2012) To resprout or not to resprout: factors driving intraspecific variability in resprouting. Oikos 121, 1577–1584.
| To resprout or not to resprout: factors driving intraspecific variability in resprouting.Crossref | GoogleScholarGoogle Scholar |
Ojeda F (1998) Biogeography of seeder and resprouter Erica species in the Cape Floristic Region – where are the resprouters? Biological Journal of the Linnean Society 63, 331–347.
| Biogeography of seeder and resprouter Erica species in the Cape Floristic Region – where are the resprouters?Crossref | GoogleScholarGoogle Scholar |
Ojeda F, Brun FG, Vergara JJ (2005) Fire, rain and the selection of seeder and resprouter life-histories in fire-recruiting, woody plants. New Phytologist 168, 155–165.
| Fire, rain and the selection of seeder and resprouter life-histories in fire-recruiting, woody plants.Crossref | GoogleScholarGoogle Scholar |
Oliver EGH (1991) The Ericoideae (Ericaceae) – a review. Contributions of the Bolus Herbarium 13, 158–208.
Parra A, Moreno JM (2018) Drought differentially affects the post-fire dynamics of seeders and resprouters in a Mediterranean shrubland. Science of the Total Environment 626, 1219–1229.
| Drought differentially affects the post-fire dynamics of seeders and resprouters in a Mediterranean shrubland.Crossref | GoogleScholarGoogle Scholar |
Paula S, Pausas JG (2006) Leaf traits and resprouting ability in the mediterranean basin. Functional Ecology 20, 941–947.
| Leaf traits and resprouting ability in the mediterranean basin.Crossref | GoogleScholarGoogle Scholar |
Pausas JG, Keeley JE, Verdu M (2006) Inferring differential evolutionary processes of plant persistence traits in Northern Hemisphere Mediterranean fire-prone ecosystems. Journal of Ecology 94, 31–39.
| Inferring differential evolutionary processes of plant persistence traits in Northern Hemisphere Mediterranean fire-prone ecosystems.Crossref | GoogleScholarGoogle Scholar |
Pausas JG, Pratt RB, Keeley JE, Jacobsen AL, Ramirez AR, Vilagrosa A, Paula S, Kaneakua-Pia IN, Davis SD (2016) Towards understanding resprouting at the global scale. New Phytologist 209, 945–954.
| Towards understanding resprouting at the global scale.Crossref | GoogleScholarGoogle Scholar |
Pratt RB, Jacobsen AL, Mohla R, Ewers FW, Davis SD (2008) Linkage between water stress tolerance and life history type in seedlings of nine chaparral species (Rhamnaceae). Journal of Ecology 96, 1252–1265.
| Linkage between water stress tolerance and life history type in seedlings of nine chaparral species (Rhamnaceae).Crossref | GoogleScholarGoogle Scholar |
Pratt RB, North GB, Jacobsen AL, Ewers FW, Davis SD (2010) Xylem root and shoot hydraulics is linked to life history type in chaparral seedlings. Functional Ecology 24, 70–81.
| Xylem root and shoot hydraulics is linked to life history type in chaparral seedlings.Crossref | GoogleScholarGoogle Scholar |
Pratt RB, Jacobsen AL, Jacobs SM, Esler KJ (2012) Xylem transport safety and efficiency differ among fynbos shrub life history types and between two sites differing in mean rainfall. International Journal of Plant Sciences 173, 474–483.
| Xylem transport safety and efficiency differ among fynbos shrub life history types and between two sites differing in mean rainfall.Crossref | GoogleScholarGoogle Scholar |
Quirk J, McDowell NG, Leake JR, Hudson PJ, Beerling DJ (2013) Increased susceptibility to drought-induced mortality in Sequoia sempervirens (Cupressaceae) trees under Cenozoic atmospheric carbon dioxide starvation. American Journal of Botany 100, 582–591.
| Increased susceptibility to drought-induced mortality in Sequoia sempervirens (Cupressaceae) trees under Cenozoic atmospheric carbon dioxide starvation.Crossref | GoogleScholarGoogle Scholar | 23425559PubMed |
Sala A, Piper F, Hoch G (2010) Physiological mechanisms of drought-induced tree mortality are far from being resolved. New Phytologist 186, 274–281.
| Physiological mechanisms of drought-induced tree mortality are far from being resolved.Crossref | GoogleScholarGoogle Scholar |
Sala A, Woodruff DR, Meinzer FC (2012) Carbon dynamics in trees: feast or famine? Tree Physiology 32, 764–775.
| Carbon dynamics in trees: feast or famine?Crossref | GoogleScholarGoogle Scholar | 22302370PubMed |
Schumann D, Kirsten G, Oliver EGH (1992) ‘Ericas of South Africa.’ (Fernwood Press: Vlaeberg, South Africa)
Schwilk DW, Ackerly DD (2005) Is there a cost to resprouting? Seedling growth rate and drought tolerance in sprouting and nonsprouting Ceanothus (Rhamnaceae). American Journal of Botany 92, 404–410.
| Is there a cost to resprouting? Seedling growth rate and drought tolerance in sprouting and nonsprouting Ceanothus (Rhamnaceae).Crossref | GoogleScholarGoogle Scholar | 21652416PubMed |
Segarra-Moaragues JG, Ojeda F (2010) Postfire response and genetic diversity in Erica coccinea: connecting population dynamics and diversification in a biodiversity hotspot. Evolution 64, 3511–3524.
| Postfire response and genetic diversity in Erica coccinea: connecting population dynamics and diversification in a biodiversity hotspot.Crossref | GoogleScholarGoogle Scholar |
Sevanto S, McDowell NG, Dickman LT, Pangle R, Pockman WT (2014) How do trees die? A test of the hydraulic failure and carbon starvation hypotheses. Plant, Cell & Environment 37, 153–161.
| How do trees die? A test of the hydraulic failure and carbon starvation hypotheses.Crossref | GoogleScholarGoogle Scholar |
Skelton RP, West AG, Dawson TE (2015) Predicting plant vulnerability to drought in biodiverse regions using functional traits. Proceedings of the National Academy of Sciences 112, 5744–5749.
| Predicting plant vulnerability to drought in biodiverse regions using functional traits.Crossref | GoogleScholarGoogle Scholar |
Tucker CM, Rebelo AG, Manne LL (2012) Contribution of disturbance to distribution and abundance in a fire-adapted system. Ecography 35, 348–355.
| Contribution of disturbance to distribution and abundance in a fire-adapted system.Crossref | GoogleScholarGoogle Scholar |
van Blerk JJ, West AG, Altwegg R, Hoffman MT (2021) Post-fire summer rainfall differentially affects reseeder and resprouter population recovery in fire-prone shrublands of South Africa. Science of the Total Environment 788, 147699
| Post-fire summer rainfall differentially affects reseeder and resprouter population recovery in fire-prone shrublands of South Africa.Crossref | GoogleScholarGoogle Scholar |
van Wilgen BW, Richardson DM, Kruger FJ, van Hensbergen HJ (1992) ‘Fire in South African Mountain Fynbos.’ Ecological studies. p. 325. (Springer Verlag: Berlin, Germany)
van Wilgen BW, Forsyth GG, De Klerk H, Das S, Khuluse S, Schmitz P (2010) Fire management in Mediterranean-climate shrublands: a case study from the Cape fynbos, South Africa. Journal of Applied Ecology 47, 631–638.
| Fire management in Mediterranean-climate shrublands: a case study from the Cape fynbos, South Africa.Crossref | GoogleScholarGoogle Scholar |
Verdaguer D, Ojeda F (2002) Root starch storage and allocation patterns in seeder and resprouter seedlings of two Cape Erica (Ericaceae) species. American Journal of Botany 89, 1189–1196.
| Root starch storage and allocation patterns in seeder and resprouter seedlings of two Cape Erica (Ericaceae) species.Crossref | GoogleScholarGoogle Scholar | 21665719PubMed |
Verdú M (2000) Ecological and evolutionary differences between Mediterranean seeders and resprouters. Journal of Vegetation Science 11, 265–268.
| Ecological and evolutionary differences between Mediterranean seeders and resprouters.Crossref | GoogleScholarGoogle Scholar |
Vilagrosa A, Hernández EI, Luis VC, Cochard H, Pausas JG (2014) Physiological differences explain the co-existence of different regeneration strategies in Mediterranean ecosystems. New Phytologist 201, 1277–1288.
| Physiological differences explain the co-existence of different regeneration strategies in Mediterranean ecosystems.Crossref | GoogleScholarGoogle Scholar |
West AG, Dawson TE, February EC, Midgley GF, Bond WJ, Aston TL (2012) Diverse functional responses to drought in a Mediterranean-type shrubland in South Africa. New Phytologist 195, 396–407.
| Diverse functional responses to drought in a Mediterranean-type shrubland in South Africa.Crossref | GoogleScholarGoogle Scholar |