Phytophagous Insects Reduce Cycad Resistance to Tropical Cyclone Winds and Impair Storm Recovery

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Tropical cyclones (TCs) are large-scale natural disturbances that affect the health of managed and unmanaged forests, the urban landscape, and perennial horticulture plantings for many years after the disturbance. Numerous post-TC assessments reveal that tree species vary in damage and recovery dynamics. Guam experiences more TCs than any other state or territory of the United States (Marler, 2001). Tropical cyclones are called typhoons in the western Pacific Ocean, and the island’s forests have been dubbed “typhoon forests” because general appearance at any time is defined by the most recent typhoons (Stone, 1971).

Native tree species possess traits that enable them to recover after TC damage, which is one reason that these species with aesthetic appeal are ideal for horticultural applications. Cycas micronesica K.D. Hill was the most abundant tree species in Guam as recently as 2002 (Donnegan et al., 2004). The pachycaulous stems of this species are non-woody, and stem sections that are broken off during TC damage readily develop adventitious roots and continue growing (Fig. 1A). The species is recognized for its ability to recover from damage after a TC. For example, reliance on C. micronesica tissues for human consumption was historically important after frequent TCs that destroyed other crop plants, primarily because concurrent damage to C. micronesica was minimal (Edwards, 1918).

Fig. 1.
Fig. 1.

Before the buildup of alien herbivore populations in Guam, a Cycas micronesica tree snapped by tropical cyclone winds survived with no threats. (A) The snapped portion of the stem developed adventitious roots and continued growth. (B) The intact base of the stem developed adventitious stems and continued growth. (C) Early development of an adventitious bud. (D) Feral pig populations increased by the time of Typhoon Paka in 1997, consuming 100% of the snapped portion of the stems.

Citation: HortScience horts 48, 10; 10.21273/HORTSCI.48.10.1224

We quantified damage to the C. micronesica population when peak winds of 298 wind km·h−1 impacted Guam during Typhoon Paka in Dec. 1997 (Marler and Hirsh, 1998) and determined that mechanical failure from TC winds snapped stems in ≈12% of the trees. We then followed recovery of plants that experienced various damage categories until 1999 (Hirsh and Marler, 2002) and determined that 100% of the intact lower stems recovered (Fig. 1B) by formation of adventitious stems on the stump (Fig. 1C), but 100% of the toppled portion of the stems was consumed by feral pigs (Sus scrofa L.; Fig. 1D).

Comparing Two Tropical Cyclones

Typhoon Chaba passed north of Guam in Aug. 2004, bringing peak wind speeds less than half of those in Typhoon Paka. We noticed that the proportion of C. micronesica trees exhibiting mechanical failure during this TC appeared to surpass the damage documented during the more powerful Typhoon Paka. To verify that our observations were accurate, we recorded status of all C. micronesica trees along a transect in northwest Guam until we exceeded 300 trees. The less intense winds from Typhoon Chaba indeed caused 18% of the trees to fail by stem breakage. Therefore, we set out to determine how a TC with moderate wind speeds could impose greater mechanical damage to a highly resistant tree species than a more powerful TC only 7 years prior. Furthermore, we monitored recovery of all plants on the transect by observations conducted every 6 months until 2009 when mortality reached 100% for the trees that were snapped in Typhoon Chaba.

During Typhoon Paka, we noticed that ≈60% of the trees that failed mechanically were supporting large epiphytes such as Polypodium L. at the time of the TC (Table 1; Fig. 1B). Therefore, we observed all snapped trees after Typhoon Chaba to determine that none of them supported large epiphytes. During Typhoon Paka, we noticed that the internal stem tissue of snapped stems was healthy at the height of mechanical failure. However, almost 90% of the snapped trees in Typhoon Chaba exhibited internal tissue decay at the height of mechanical failure (Table 1; Fig. 1A). During Typhoon Paka, 100% of the stems that failed had fallen in the direction of the maximum wind vector. However, in Typhoon Chaba, approximately half of the stems that failed had fallen in a direction that deviated from the maximum wind vector (Table 1). We did not correlate stem diameter with biomechanical failure in Typhoon Paka. However, for the trees in our observations after Typhoon Chaba, diameter did not appear to be a factor because the trees that did not fail exhibited a mean of 28.4 cm basal diameter and the trees that failed exhibited a mean of 31.9 cm basal diameter. After Typhoon Paka, 100% of the stem sections that failed was subsequently consumed by feral pigs, but 100% of the intact part of the stem sections developed adventitious buds and recovered. After Typhoon Chaba, the toppled stem sections for trees that failed met the same fate as those from Typhoon Paka. Furthermore, 100% of the intact stem sections were subsequently killed by Aulacaspis yasumatsui Takagi infestations. Therefore, Typhoon Paka resulted in high resilience and no mortality of the trees in this damage category, but Typhoon Chaba resulted in low resilience and 100% mortality of the trees in the same damage category.

Table 1.

Comparison of Guam’s Cycas micronesica population responses to the powerful tropical cyclone Paka in 1997 and the less intense tropical cyclone Chaba in 2004.

Table 1.

Applications

A tree’s resistance to TC damage may be realized by minimizing the mechanical forces encountered by the tree, an avoidance strategy, or by resisting breakage while encountering the mechanical forces, a tolerance strategy. Plants may exhibit a tradeoff between avoidance and tolerance strategies (Puijalon et al., 2011), but all woody forest species may not conform to this tradeoff (Butler et al., 2011). The ability to recover from damage imposed by a disturbance such as a TC is termed resilience (see Holling, 1973).

These factors have been studied extensively for TCs in many geographic locations. A serendipitous approach is generally exploited as a result of the stochastic nature of the large-scale disturbances. Ecologists and horticulturists may seize the opportunity to secure information about vegetation damage and recovery after a TC that damages orchards or natural habitats in which they conduct their research. Rarely are pre-TC vegetation or habitat data reported in a manner that informs the interpretations of damage and recovery.

We are unaware of other reports that focus on how a single tree species is damaged by sequential TCs in the same geographic location. The following observations may be useful for a better understanding of how invasion biology interacts with large-scale abiotic disturbances to influence perennial tree species.

  • The epiphyte load that elicited most of the stem failures in Typhoon Paka enabled the damage by compromising the ability of C. micronesica canopy to avoid wind drag. The stem decay that elicited most of the stem failures in Typhoon Chaba enabled the damage by reducing the tolerance of C. micronesica stems to external mechanical forces.

  • Stem decay was a consequence of earlier damage by the native stem borer Dihammus marianarum Aurivillius (Marler and Muniappan, 2006). Stem borer species cause copious economic and ecological damage worldwide and are known to possess the ability to overwhelm trees in suboptimal health (Hlásny and Turčáni, 2013). Increased damage to sugar cane by a relatively minor cyclone in Mauritius was similarly attributed to stem borer feeding that predisposed the plants to damage (Waister, 1972).

  • The invasions of Aulacaspis yasumatsui in 2003 (Marler and Muniappan, 2006) and Chilades pandava Horsfield in 2005 (Moore et al., 2005) have threatened the C. micronesica trees in commercial and residential landscapes and natural forests (Marler and Lawrence, 2012). These pests were responsible for the 100% mortality of the intact portions of the snapped stems during the 5 years after Typhoon Chaba.

  • Ultimate mortality of the intact stem sections was a tritrophic phenomenon. We introduced the scale predator Rhyzobius lophanthae Blaisdell in 2005 (Moore et al., 2005) and have recently discovered that this beetle avoids its prey-infesting leaves close to ground level (Marler et al., 2013). The adventitious buds on the intact stem sections that remained after the Typhoon Chaba stem failures were chronically infested by A. yasumatsui, and predation was minimal because of this unusual behavior of the predator. Many of the trees in our transect that did not experience stem failure during Typhoon Chaba were adequately protected from scale infestations by R. lophanthae, because most or all of their leaves were positioned at higher elevations where the predator feeds effectively.

  • All of the snapped stems that fell in a direction that deviated from maximum wind vector in Typhoon Chaba exhibited cortex tissue decay that was 180° from the direction of the fall direction (e.g., Fig. 2A). These observations indicate an intact cortex is critical for tolerating the forces imposed on this pachycaulous stem by wind drag and that the effect occurs by countering tension stress rather than countering compression stress.

  • Trees with diseased roots or stems are generally more susceptible than healthy trees to wind damage (Landis and Evans, 1974; Putz et al., 1983; Shaw and Taes, 1977; Whitney et al., 2002). Tissue defects compromise mechanical strength of tree stems and add to complications of accurate assessment of windthrow risk (Ruel et al., 2010). Bark damage by deer browsing increased wind damage of coniferous trees by causing subsequent wood decay (Shibita and Torazawa, 2008). Our observations indicate that an understanding of initial factors that generate stem defects would improve assessment of ultimate wind damage risks. The pachycaulous, parenchymatous Cycas stem is highly susceptible to secondary decomposition of tissues when the cortex tissues are exposed after damage to bark (Fisher et al., 2009).

  • Resprouting on snapped tree trunks is called “direct regeneration” because it enables re-establishment of the pre-disturbance plant composition without recruitment of new individuals (Boucher et al., 1994). This direct regeneration of C. micronesica trees after Guam’s numerous historical TCs undoubtedly enabled the species to sustain its status as the most abundant tree through 2002 (Donnegan et al., 2004).

  • Arborescent palm species also exhibit a pachycaulous stem and simple architecture and vary in damage and recovery to TCs (Griffith et al., 2008). However, stem construction tissues and their internal organization are highly contrasting between palms and cycads (see Norstog and Nicholls, 1997; Tomlinson, 2006). Further study of the unique stem features of these two important plant groups may improve our understanding of similarities and differences in TC resistance and resilience.

  • This study underscores the fact that many years of observations after TCs are required to accurately determine resilience. Had we ended our surveys shortly after Typhoon Chaba when we noticed the adventitious stem development on the intact stem sections of failed trees, we would have inaccurately attributed 100% recovery to the trees in this damage category. This facet of studying plant recovery after natural disturbances is not restricted to TC damage (Rogers, 1985).

  • A span of less than one decade allowed two alien invasions to eliminate the incipient resilience of a native tree species to TC damage.

Fig. 2.
Fig. 2.

Cycas micronesica stem failures increased in incidence during Typhoon Chaba in 2004. (A) Damaged stem tissue after stem borer damage was associated with most of the broken stems in Typhoon Chaba. (B) Trees burdened by large epiphytes such as this Polypodium accounted for most stem failures in Typhoon Paka. (C) Mechanical failure of a tree during Typhoon Chaba in 2004. (D) The same tree in 2009 showing removal of the snapped portion of the stem by pig herbivory, mortality of the intact stem base by phytophagous insect infestations, and mortality of all seedlings by Aulacaspis yasumatsui herbivory.

Citation: HortScience horts 48, 10; 10.21273/HORTSCI.48.10.1224

Literature Cited

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    • Search Google Scholar
    • Export Citation
  • ButlerD.W.GleasonS.M.DavidsonI.OnodaY.WestobyM.2011Safety and streamlining of woody shoots in wind: An empirical study across 39 species in tropical AustraliaNew Phytol.193137149

    • Search Google Scholar
    • Export Citation
  • DonneganJ.A.ButlerS.L.GrabowieckiW.HiseroteB.A.LimtiacoD.2004Guam’s forest resources 2002. Resource Bulletin PNW-RB-243. U.S. Department of Agriculture Forest Service Pacific Northwest Research Station Portland OR. 32 pp

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  • GriffithM.P.NoblickL.R.DoweJ.L.HusbyC.E.CalonjeM.2008Cyclone tolerance in New World Arecaceae: Biogeographic variation and abiotic natural selectionAnn. Bot. (Lond.)102591598

    • Search Google Scholar
    • Export Citation
  • HirshH.MarlerT.2002Damage and recovery of Cycas micronesica after Typhoon PakaBiotropica34598602

  • HlásnyT.TurčániM.2013Persisting bark beetle outbreak indicates the unsustainability of secondary Norway spruce forests: Case study from Central EuropeAnn. For. Sci.70481491

    • Search Google Scholar
    • Export Citation
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    • Search Google Scholar
    • Export Citation
  • MarlerT.E.MillerR.MooreA.2013Vertical stratification of predation on Aulacaspis yasumatsui infesting Cycas micronesica seedlingsHortScience486062

    • Search Google Scholar
    • Export Citation
  • MarlerT.E.MuniappanR.2006Pests of Cycas micronesica: Leaf, stem, and male reproductive tissues with notes on current threat statusMicronesica3919

    • Search Google Scholar
    • Export Citation
  • MooreA.MarlerT.MillerR.H.MuniappanR.2005Biological control of cycad aulacaspis scale on GuamThe Cycad Newsletter2868

  • NorstogK.J.NichollsT.J.1997The biology of the cycads. Cornell Univ. Press Ithica NY

  • PuijalonS.BoumaT.J.DouadyC.J.van GroenendaelJ.AntenN.P.R.MartelE.BornetteG.2011Plant resistance to mechanical stress: Evidence of an avoidance–tolerance trade-offNew Phytol.19111411149

    • Search Google Scholar
    • Export Citation
  • PutzF.E.ColeyP.D.LuK.MontalvoA.AielloA.1983Uprooting and snapping of trees: Structural determinants and ecological consequencesCan. J. For. Res.1310111020

    • Search Google Scholar
    • Export Citation
  • RogersG.F.1985Mortality of burned Cereus giganteusEcology66630632

  • RuelJ.-C.AchimA.HerreraR.E.CloutierA.2010Relating mechanical strength at the stem level to values obtained from defect-free wood samplesTrees (Berl.)2411271135

    • Search Google Scholar
    • Export Citation
  • ShawC.G.IIITaesE.H.A.1977Impact of Dothistroma needle blight and Armillaria root rot on diameter growth of Pinus radiataPhytopathology6613191323

    • Search Google Scholar
    • Export Citation
  • ShibitaE.TorazawaY.2008Effects of bark stripping by sika deer, Cervus nippon, on wind damage to coniferous trees in subalpine forest of central JapanJ. For. Res.13296301

    • Search Google Scholar
    • Export Citation
  • StoneB.C.1971America's Asiatic flora: the plants of GuamAmerican Scientist59308319

  • TomlinsonP.B.2006The uniqueness of palmsBot. J. Linn. Soc.151514

  • WaisterP.D.1972Wind damage in horticultural cropsHorticultural Abstracts42609615

  • WhitneyR.D.FlemingR.L.ZhouK.MossaD.S.2002Relationship of root rot to black spruce windfall and mortality following strip clear-cuttingCan. J. For. Res.32283294

    • Search Google Scholar
    • Export Citation

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Contributor Notes

Support provided by U.S. Forest Service Project No. 06-DG-11052021-206 and No. 09-DG-11052021-173.

To whom reprint requests should be addressed; e-mail tmarler@uguam.uog.edu.

Headings

Figures

  • View in gallery

    Before the buildup of alien herbivore populations in Guam, a Cycas micronesica tree snapped by tropical cyclone winds survived with no threats. (A) The snapped portion of the stem developed adventitious roots and continued growth. (B) The intact base of the stem developed adventitious stems and continued growth. (C) Early development of an adventitious bud. (D) Feral pig populations increased by the time of Typhoon Paka in 1997, consuming 100% of the snapped portion of the stems.

  • View in gallery

    Cycas micronesica stem failures increased in incidence during Typhoon Chaba in 2004. (A) Damaged stem tissue after stem borer damage was associated with most of the broken stems in Typhoon Chaba. (B) Trees burdened by large epiphytes such as this Polypodium accounted for most stem failures in Typhoon Paka. (C) Mechanical failure of a tree during Typhoon Chaba in 2004. (D) The same tree in 2009 showing removal of the snapped portion of the stem by pig herbivory, mortality of the intact stem base by phytophagous insect infestations, and mortality of all seedlings by Aulacaspis yasumatsui herbivory.

References

  • BoucherD.H.VandermeerJ.H.MallonaM.A.ZamoraN.PerfectoI.1994Resistance and resilience in a directly regenerating rainforest: Nicaraguan trees of the Vochysiaceae after Hurricane JoanFor. Ecol. Mgt.68127136

    • Search Google Scholar
    • Export Citation
  • ButlerD.W.GleasonS.M.DavidsonI.OnodaY.WestobyM.2011Safety and streamlining of woody shoots in wind: An empirical study across 39 species in tropical AustraliaNew Phytol.193137149

    • Search Google Scholar
    • Export Citation
  • DonneganJ.A.ButlerS.L.GrabowieckiW.HiseroteB.A.LimtiacoD.2004Guam’s forest resources 2002. Resource Bulletin PNW-RB-243. U.S. Department of Agriculture Forest Service Pacific Northwest Research Station Portland OR. 32 pp

  • EdwardsC.W.1918Report of the Guam Agricultural Experiment Station. Government Printing Office Washington DC

  • FisherJ.B.LindströmA.MarlerT.2009Tissue responses and solution movement after stem wounding in six Cycas speciesHortScience44848851

  • GriffithM.P.NoblickL.R.DoweJ.L.HusbyC.E.CalonjeM.2008Cyclone tolerance in New World Arecaceae: Biogeographic variation and abiotic natural selectionAnn. Bot. (Lond.)102591598

    • Search Google Scholar
    • Export Citation
  • HirshH.MarlerT.2002Damage and recovery of Cycas micronesica after Typhoon PakaBiotropica34598602

  • HlásnyT.TurčániM.2013Persisting bark beetle outbreak indicates the unsustainability of secondary Norway spruce forests: Case study from Central EuropeAnn. For. Sci.70481491

    • Search Google Scholar
    • Export Citation
  • HollingC.S.1973Resilience and stability of ecological systemsAnnu. Rev. Ecol. Syst.4123

  • LandisT.D.EvansA.K.1974A relationship between Fomes applanatus and Aspen windthrowPlant Disease Reporter58110113

  • MarlerT.E.2001Tropical cyclones and perennial species in the Mariana IslandsHortScience36264268

  • MarlerT.E.HirshH.1998Guam’s Cycas micronesica population ravaged by Supertyphoon PakaHortScience3311161118

  • MarlerT.E.LawrenceJ.H.2012Demography of Cycas micronesica on Guam following introduction of the armoured scale Aulacaspis yasumatsuiJ. Trop. Ecol.28233242

    • Search Google Scholar
    • Export Citation
  • MarlerT.E.MillerR.MooreA.2013Vertical stratification of predation on Aulacaspis yasumatsui infesting Cycas micronesica seedlingsHortScience486062

    • Search Google Scholar
    • Export Citation
  • MarlerT.E.MuniappanR.2006Pests of Cycas micronesica: Leaf, stem, and male reproductive tissues with notes on current threat statusMicronesica3919

    • Search Google Scholar
    • Export Citation
  • MooreA.MarlerT.MillerR.H.MuniappanR.2005Biological control of cycad aulacaspis scale on GuamThe Cycad Newsletter2868

  • NorstogK.J.NichollsT.J.1997The biology of the cycads. Cornell Univ. Press Ithica NY

  • PuijalonS.BoumaT.J.DouadyC.J.van GroenendaelJ.AntenN.P.R.MartelE.BornetteG.2011Plant resistance to mechanical stress: Evidence of an avoidance–tolerance trade-offNew Phytol.19111411149

    • Search Google Scholar
    • Export Citation
  • PutzF.E.ColeyP.D.LuK.MontalvoA.AielloA.1983Uprooting and snapping of trees: Structural determinants and ecological consequencesCan. J. For. Res.1310111020

    • Search Google Scholar
    • Export Citation
  • RogersG.F.1985Mortality of burned Cereus giganteusEcology66630632

  • RuelJ.-C.AchimA.HerreraR.E.CloutierA.2010Relating mechanical strength at the stem level to values obtained from defect-free wood samplesTrees (Berl.)2411271135

    • Search Google Scholar
    • Export Citation
  • ShawC.G.IIITaesE.H.A.1977Impact of Dothistroma needle blight and Armillaria root rot on diameter growth of Pinus radiataPhytopathology6613191323

    • Search Google Scholar
    • Export Citation
  • ShibitaE.TorazawaY.2008Effects of bark stripping by sika deer, Cervus nippon, on wind damage to coniferous trees in subalpine forest of central JapanJ. For. Res.13296301

    • Search Google Scholar
    • Export Citation
  • StoneB.C.1971America's Asiatic flora: the plants of GuamAmerican Scientist59308319

  • TomlinsonP.B.2006The uniqueness of palmsBot. J. Linn. Soc.151514

  • WaisterP.D.1972Wind damage in horticultural cropsHorticultural Abstracts42609615

  • WhitneyR.D.FlemingR.L.ZhouK.MossaD.S.2002Relationship of root rot to black spruce windfall and mortality following strip clear-cuttingCan. J. For. Res.32283294

    • Search Google Scholar
    • Export Citation

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