HORTSCIENCE 48(10):1224–1226. 2013.

Phytophagous Insects Reduce CycadResistance to Tropical Cyclone Windsand Impair Storm RecoveryThomas E. Marler1

Western Pacific Tropical Research Center, College of Natural and AppliedSciences, University of Guam, UOG Station, Mangilao, Guam 96923

John H. LawrenceU.S. Department of Agriculture, Natural Resources Conservation Service,Barrigada, Guam 96913

Additional index words. biomechanics, Cycas micronesica, Guam, mechanical stress, stemborer, wind damage

Tropical cyclones (TCs) are large-scalenatural disturbances that affect the health ofmanaged and unmanaged forests, the urbanlandscape, and perennial horticulture plant-ings for many years after the disturbance.Numerous post-TC assessments reveal thattree species vary in damage and recoverydynamics. Guam experiences more TCs thanany other state or territory of the UnitedStates (Marler, 2001). Tropical cyclones arecalled typhoons in the western Pacific Ocean,and the island’s forests have been dubbed‘‘typhoon forests’’ because general appear-ance at any time is defined by the most recenttyphoons (Stone, 1971).

Native tree species possess traits thatenable them to recover after TC damage,which is one reason that these species withaesthetic appeal are ideal for horticulturalapplications. Cycas micronesica K.D. Hillwas the most abundant tree species in Guamas recently as 2002 (Donnegan et al., 2004).The pachycaulous stems of this species arenon-woody, and stem sections that are brokenoff during TC damage readily develop ad-ventitious roots and continue growing (Fig.1A). The species is recognized for its abilityto recover from damage after a TC. Forexample, reliance on C. micronesica tissuesfor human consumption was historically im-portant after frequent TCs that destroyedother crop plants, primarily because concur-rent damage to C. micronesica was minimal(Edwards, 1918).

We quantified damage to the C. micro-nesica population when peak winds of 298wind km·h–1 impacted Guam during Ty-phoon Paka in Dec. 1997 (Marler and Hirsh,1998) and determined that mechanical fail-ure from TC winds snapped stems in �12%of the trees. We then followed recoveryof plants that experienced various damage

categories until 1999 (Hirsh and Marler,2002) and determined that 100% of theintact lower stems recovered (Fig. 1B) byformation of adventitious stems on the stump(Fig. 1C), but 100% of the toppled portion ofthe stems was consumed by feral pigs (Susscrofa L.; Fig. 1D).

Comparing Two Tropical Cyclones

Typhoon Chaba passed north of Guam inAug. 2004, bringing peak wind speeds lessthan half of those in Typhoon Paka. Wenoticed that the proportion of C. micronesica

trees exhibiting mechanical failure duringthis TC appeared to surpass the damagedocumented during the more powerful Ty-phoon Paka. To verify that our observationswere accurate, we recorded status of allC. micronesica trees along a transect in north-west Guam until we exceeded 300 trees. Theless intense winds from Typhoon Chaba in-deed caused 18% of the trees to fail by stembreakage. Therefore, we set out to determinehow a TC with moderate wind speeds couldimpose greater mechanical damage to ahighly resistant tree species than a more pow-erful TC only 7 years prior. Furthermore,we monitored recovery of all plants on thetransect by observations conducted every 6months until 2009 when mortality reached100% for the trees that were snapped inTyphoon Chaba.

During Typhoon Paka, we noticed that�60% of the trees that failed mechanicallywere supporting large epiphytes such asPolypodium L. at the time of the TC (Table 1;Fig. 1B). Therefore, we observed all snappedtrees after Typhoon Chaba to determine thatnone of them supported large epiphytes.During Typhoon Paka, we noticed that theinternal stem tissue of snapped stems washealthy at the height of mechanical failure.However, almost 90% of the snapped treesin Typhoon Chaba exhibited internal tissuedecay at the height of mechanical failure(Table 1; Fig. 1A). During Typhoon Paka,100% of the stems that failed had fallen inthe direction of the maximum wind vector.

Fig. 1. Before the buildup of alien herbivore populations in Guam, a Cycas micronesica tree snapped bytropical cyclone winds survived with no threats. (A) The snapped portion of the stem developedadventitious roots and continued growth. (B) The intact base of the stem developed adventitious stemsand continued growth. (C) Early development of an adventitious bud. (D) Feral pig populationsincreased by the time of Typhoon Paka in 1997, consuming 100% of the snapped portion of the stems.

Received for publication 11 July 2013. Acceptedfor publication 15 Aug. 2013.Support provided by U.S. Forest Service Project No.06-DG-11052021-206 and No. 09-DG-11052021-173.1To whom reprint requests should be addressed;e-mail tmarler@uguam.uog.edu.

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However, in Typhoon Chaba, approximatelyhalf of the stems that failed had fallen ina direction that deviated from the maximum

wind vector (Table 1). We did not correlatestem diameter with biomechanical failure inTyphoon Paka. However, for the trees in ourobservations after Typhoon Chaba, diameterdid not appear to be a factor because the treesthat did not fail exhibited a mean of 28.4 cmbasal diameter and the trees that failedexhibited a mean of 31.9 cm basal diameter.After Typhoon Paka, 100% of the stemsections that failed was subsequently con-sumed by feral pigs, but 100% of the intactpart of the stem sections developed adventi-tious buds and recovered. After TyphoonChaba, the toppled stem sections for trees thatfailed met the same fate as those fromTyphoon Paka. Furthermore, 100% of the

intact stem sections were subsequently killedby Aulacaspis yasumatsui Takagi infestations.Therefore, Typhoon Paka resulted in highresilience and no mortality of the trees in thisdamage category, but Typhoon Chaba resultedin low resilience and 100% mortality of thetrees in the same damage category.

Applications

A tree’s resistance to TC damage may berealized by minimizing the mechanical forcesencountered by the tree, an avoidance strat-egy, or by resisting breakage while encoun-tering the mechanical forces, a tolerancestrategy. Plants may exhibit a tradeoff be-tween avoidance and tolerance strategies(Puijalon et al., 2011), but all woody forestspecies may not conform to this tradeoff(Butler et al., 2011). The ability to recoverfrom damage imposed by a disturbance suchas a TC is termed resilience (see Holling, 1973).

These factors have been studied exten-sively for TCs in many geographic locations.A serendipitous approach is generally exploitedas a result of the stochastic nature of the large-scale disturbances. Ecologists and horticul-turists may seize the opportunity to secureinformation about vegetation damage andrecovery after a TC that damages orchardsor natural habitats in which they conduct theirresearch. Rarely are pre-TC vegetation orhabitat data reported in a manner that informsthe interpretations of damage and recovery.

We are unaware of other reports that focuson how a single tree species is damaged bysequential TCs in the same geographiclocation. The following observations maybe useful for a better understanding of howinvasion biology interacts with large-scaleabiotic disturbances to influence perennialtree species.

� The epiphyte load that elicited most of thestem failures in Typhoon Paka enabledthe damage by compromising the ability ofC. micronesica canopy to avoid wind drag.The stem decay that elicited most of the stemfailures in Typhoon Chaba enabled the dam-age by reducing the tolerance of C. micro-nesica stems to external mechanical forces.

� Stem decay was a consequence of earlierdamage by the native stem borer Diham-mus marianarum Aurivillius (Marler andMuniappan, 2006). Stem borer speciescause copious economic and ecologicaldamage worldwide and are known topossess the ability to overwhelm trees insuboptimal health (Hlasny and Turcani,2013). Increased damage to sugar cane bya relatively minor cyclone in Mauritiuswas similarly attributed to stem borerfeeding that predisposed the plants todamage (Waister, 1972).

� The invasions of Aulacaspis yasumatsuiin 2003 (Marler and Muniappan, 2006)and Chilades pandava Horsfield in 2005(Moore et al., 2005) have threatened theC. micronesica trees in commercial andresidential landscapes and natural forests(Marler and Lawrence, 2012). These pests

Table 1. Comparison of Guam’s Cycas micronesicapopulation responses to the powerful tropicalcyclone Paka in 1997 and the less intensetropical cyclone Chaba in 2004.

Trait Paka Chaba

Biomechanical failure (%) 12 18Heavy epiphyte load (%) 59 0Stem rot at breakage (%) 0 88Stem aligned leewardz (%) 100 53zThis was a binary decision. ‘‘Yes’’ if failed stemdirection was wind direction. ‘‘No’’ if stem directiondeviated from wind direction.

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 inTyphoon Chaba. (B) Trees burdened by large epiphytes such as this Polypodium accounted for moststem 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, mortalityof the intact stem base by phytophagous insect infestations, and mortality of all seedlings byAulacaspis yasumatsui herbivory.

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FEATURE

were responsible for the 100% mortality ofthe intact portions of the snapped stemsduring the 5 years after Typhoon Chaba.

� Ultimate mortality of the intact stem sec-tions was a tritrophic phenomenon. Weintroduced the scale predator Rhyzobiuslophanthae Blaisdell in 2005 (Mooreet al., 2005) and have recently discoveredthat this beetle avoids its prey-infestingleaves close to ground level (Marler et al.,2013). The adventitious buds on the intactstem sections that remained after the Ty-phoon Chaba stem failures were chronicallyinfested by A. yasumatsui, and predationwas minimal because of this unusual be-havior of the predator. Many of the trees inour transect that did not experience stemfailure during Typhoon Chaba were ade-quately protected from scale infestations byR. lophanthae, because most or all of theirleaves were positioned at higher elevationswhere the predator feeds effectively.

� All of the snapped stems that fell in a di-rection that deviated from maximum windvector in Typhoon Chaba exhibited cortextissue decay that was 180� from the directionof the fall direction (e.g., Fig. 2A). Theseobservations indicate an intact cortex iscritical for tolerating the forces imposed onthis pachycaulous stem by wind drag and thatthe effect occurs by countering tension stressrather than countering compression stress.

� Trees with diseased roots or stems aregenerally more susceptible than healthytrees to wind damage (Landis and Evans,1974; Putz et al., 1983; Shaw and Taes,1977; Whitney et al., 2002). Tissue defectscompromise mechanical strength of treestems and add to complications of accurateassessment of windthrow risk (Ruel et al.,2010). Bark damage by deer browsingincreased wind damage of coniferous treesby causing subsequent wood decay (Shibitaand Torazawa, 2008). Our observationsindicate that an understanding of initialfactors that generate stem defects wouldimprove assessment of ultimate wind dam-age risks. The pachycaulous, parenchy-matous Cycas stem is highly susceptible tosecondary decomposition of tissues whenthe cortex tissues are exposed after damageto bark (Fisher et al., 2009).

� Resprouting on snapped tree trunks iscalled ‘‘direct regeneration’’ because it en-ables re-establishment of the pre-disturbanceplant composition without recruitment ofnew individuals (Boucher et al., 1994).This direct regeneration of C. micronesicatrees after Guam’s numerous historicalTCs undoubtedly enabled the species to

sustain its status as the most abundant treethrough 2002 (Donnegan et al., 2004).

� Arborescent palm species also exhibita pachycaulous stem and simple architec-ture and vary in damage and recovery toTCs (Griffith et al., 2008). However, stemconstruction tissues and their internal or-ganization are highly contrasting betweenpalms and cycads (see Norstog and Nicholls,1997; Tomlinson, 2006). Further study of theunique stem features of these two importantplant groups may improve our understand-ing of similarities and differences in TCresistance and resilience.

� This study underscores the fact that manyyears of observations after TCs are requiredto accurately determine resilience. Had weended our surveys shortly after TyphoonChaba when we noticed the adventitiousstem development on the intact stem sectionsof failed trees, we would have inaccuratelyattributed 100% recovery to the trees in thisdamage category. This facet of studyingplant recovery after natural disturbances isnot restricted to TC damage (Rogers, 1985).

� A span of less than one decade allowedtwo alien invasions to eliminate the in-cipient resilience of a native tree species toTC damage.

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