darwin's naturalization hypothesis revisited

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The University of Chicago Darwin's Naturalization Hypothesis Revisited. Author(s): Curtis C. Daehler Source: The American Naturalist, Vol. 158, No. 3 (September 2001), pp. 324-330 Published by: The University of Chicago Press for The American Society of Naturalists Stable URL: http://www.jstor.org/stable/10.1086/321316 . Accessed: 15/07/2014 12:35 Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at . http://www.jstor.org/page/info/about/policies/terms.jsp . JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected]. . The University of Chicago Press, The American Society of Naturalists, The University of Chicago are collaborating with JSTOR to digitize, preserve and extend access to The American Naturalist. http://www.jstor.org This content downloaded from 46.223.108.115 on Tue, 15 Jul 2014 12:35:42 PM All use subject to JSTOR Terms and Conditions

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Page 1: Darwin's Naturalization Hypothesis Revisited

The University of Chicago

Darwin's Naturalization Hypothesis Revisited.Author(s): Curtis C. DaehlerSource: The American Naturalist, Vol. 158, No. 3 (September 2001), pp. 324-330Published by: The University of Chicago Press for The American Society of NaturalistsStable URL: http://www.jstor.org/stable/10.1086/321316 .

Accessed: 15/07/2014 12:35

Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at .http://www.jstor.org/page/info/about/policies/terms.jsp

.JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range ofcontent in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new formsof scholarship. For more information about JSTOR, please contact [email protected].

.

The University of Chicago Press, The American Society of Naturalists, The University of Chicago arecollaborating with JSTOR to digitize, preserve and extend access to The American Naturalist.

http://www.jstor.org

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Page 2: Darwin's Naturalization Hypothesis Revisited

vol. 158, no. 3 the american naturalist september 2001

Notes and CommentsDarwin’s Naturalization Hypothesis Revisited

Curtis C. Daehler*

Department of Botany, University of Hawaii at Manoa, Honolulu,Hawaii 96797

Submitted June 19, 2000; Accepted April 19, 2001

Keywords: flora, genera, Hawaiian Islands, introduced species,invasion, plants.

In The Origin of Species, Darwin (1859) drew attention toobservations by Alphonse de Candolle (1855) that florasgain by naturalization far more species belonging to newgenera than species belonging to native genera. Darwin(1859, p. 86) goes on to give a specific example: “In thelast edition of Dr. Asa Gray’s ‘Manual of the Flora of theUnited States’ … out of the 162 naturalised genera, noless than 100 genera are not there indigenous.” Darwinused these data to support his theory of intense compe-tition between congeners, described only a few pages ear-lier: “As the species of the same genus usually have, thoughby no means invariably, much similarity in habits andconstitution, and always in structure, the struggle will gen-erally be more severe between them” (1859, p. 60). Dar-win’s intriguing observations have recently attracted re-newed interest, as comprehensive lists of naturalized plantshave become available for various regions of the world.Two studies (Mack 1996; Rejmanek 1996, 1998) have con-cluded that naturalized floras provide some support forDarwin’s hypothesis, but only one of these studies usedstatistical tests. Analyses of additional floras are needed totest the generality of Darwin’s naturalization hypothesis.

Mack (1996) tabulated data from six regional floraswithin the United States and noted that naturalized speciesmore often belong to alien genera than native genera, withthe curious exception of one region (New York). In ad-dition to the possibility of strong competition betweennative and introduced congeners, Mack (1996) proposedthat specialist native herbivores, or pathogens, may be

* E-mail: [email protected].

Am. Nat. 2001. Vol. 158, pp. 324–330. � 2001 by The University of Chicago.0003-0147/2001/15803-0010$03.00. All rights reserved.

more likely to attack introduced species that have nativecongeners. While the raw numbers provided by Mack(1996) and Darwin (1859) may appear to support theidea that species from alien genera are more likely to nat-uralize, they do not take into account the relative numbersof species from native versus alien genera that couldhave been introduced. Thus, it is difficult to determinewhether the observed pattern differs from what would beexpected if a random subset of introductions had becomenaturalized.

To account for the number of species available for in-troduction from native versus alien genera, Rejmanek(1996, 1998) compared the number of naturalized Euro-pean grass species in California belonging to genera nativeto California with the total number of grass species nativeto Europe. He determined that European grasses natu-ralized in California are statistically more likely to belongto alien genera than expected from a random pool ofEuropean grasses. Analyses of two other families (Aster-aceae and Brassicaceae) yielded similar results, as did apreliminary analysis of some families in the Australianflora (Rejmanek 1998). These reports are a first step towarda more rigorous evaluation of Darwin’s naturalization hy-pothesis, but additional statistical tests based on other flo-ras are needed to determine whether the patterns observedin the California flora are representative of other regions.If the underrepresentation of naturalized species in nativegenera is found to be general, then this phenomenon couldpotentially lead to statistically based rules that help usunderstand the assembly of invaded communities. How-ever, if the phenomenon occurs only in certain regions orcommunities, then we are left with questions about howand why forces structuring communities differ from placeto place.

To evaluate Darwin’s naturalization hypothesis using anentire flora, I tested whether naturalized alien plant speciesin the Hawaiian Islands are more likely to belong to aliengenera than would be expected if a random pool of specieshad become naturalized. As a second test of Darwin’s hy-pothesis, I also compared the generic affinities of earlynaturalizations (pre-1900) with more recent naturaliza-

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Page 3: Darwin's Naturalization Hypothesis Revisited

Notes and Comments 325

tions to determine whether recent naturalizations weremore likely to belong to genera that had not yet becomenaturalized. The main motivation behind this second com-parison was that both early and later naturalizationstended to be introduced into the same human-impacted(mostly lowland) sites, increasing the potential for directinteractions among them (e.g., competition); native spe-cies may have been only a minor component of the veg-etation in these areas (Cuddihy and Stone 1990). Fur-thermore, a comparison of early versus later naturalizedspecies also serves to standardize for human biases thatmay have favored deliberate plants introductions that wereunusually distinct from indigenous plants in terms ofphysical appearance, benefit to humans, or ecological traits(Lyon 1929; Ewel et al. 1999). A species pool biased inthis way is expected to contain few native genera to beginwith, but a comparison of the generic affinities of earlyversus later naturalizations circumvents this problem. Fi-nally, I compared early and later naturalizations amongaccidentally introduced species to determine whether thepattern was consistent with that of the naturalized floraas a whole. The pool of accidental introductions is prob-ably not biased by human whims but is instead biasedtoward species that possess traits making them good hitch-hikers with humans. If each three of these comparisonsfail to support Darwin’s naturalization hypothesis, thenwe should consider other mechanisms besides biotic re-sistance that could be of greater importance in shapingnaturalized floras.

Methods

Native and Naturalized Floras of theHawaiian Islands

I used Wagner et al. (1999) to identify all genera of flow-ering plants native to the Hawaiian Islands. I then com-pared these native genera to the generic affinities of well-naturalized species in the Hawaiian Islands. I excludednaturalized species with very confined distributions (e.g.,those found in a single valley on a single island) becauseof the difficulty in interpreting this condition. A localizedalien might be an aggressive invader that simply has notbeen present long enough to become widespread. But analternative interpretation is that localized aliens have beenblocked from widespread naturalization by the establishedflora. Because these different possibilities lead to oppositeinterpretations with respect to Darwin’s naturalization hy-pothesis, only well-naturalized species were used for anal-yses. I used Wester (1992) and Wagner et al. (1999) asstarting points for assembling the naturalized floweringplants data set. These works list all species that have beendocumented as naturalized in Hawaii (usually from her-

barium specimens), as well as some common species thatare probably not naturalized (e.g., some Eucalyptus spp.).From this comprehensive list, I screened for only “well-naturalized” species, arbitrarily defined as species beingnaturalized on at least two different islands or, if natu-ralized only on one island, species that were naturalizedin at least three separate geographic locations within thatisland. A total of 660 alien species met these criteria forbeing well naturalized.

Comparing Naturalized Species inNative and Alien Genera

Following Rejmanek (1996, 1998), comparisons of the ob-served versus expected number of naturalized species innative genera were made at the family level, pooling mul-tiple genera within families. This approach was necessarybecause individual genera rarely contained enough natu-ralized species for statistical testing. For each family, I de-termined the following: t is the total number of naturalizedspecies in the family; n is the number of naturalized speciesbelonging to genera native to the Hawaiian Islands; a isthe number of aliens belonging to native genera availableto invade, which is equal to the global number of speciesin genera native to the Hawaiian Islands minus the numberof native Hawaiian species from those genera; f is thenumber of species in the family that were available toinvade, which is equal to the total number of species inthe family worldwide minus the total number of speciesin the family that are native to the Hawaiian Islands.

Using these variables, the expected number of natural-ized aliens belonging to native . I includedgenera p t(a/f )all species in the family (worldwide) when considering thespecies available to invade because the current naturalizedHawaiian flora is well represented by species from all themain continents of the world (Wester 1992). There is nocompelling evidence that today’s naturalized flora is dis-proportionately represented by one region of the world.Finally, I used the binomial probability distribution to de-termine whether the observed number of naturalized spe-cies in native genera was significantly less than expecteddue to chance:

tn

x (t�x)P(n) p (a/f ) (1 � a/f ) ,� ( )xp0 x

where P(n) is the probability of observing n or fewer nat-uralized species in native genera given t naturalizations. Ifthe observed number of naturalized species in native gen-era was greater than the expected number, I used the bi-nomial probability distribution to test the statistical sig-

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326 The American Naturalist

Table 1: Families native to the Hawaiian Islands with sufficientnaturalized species to detect potentially significant over- or un-derrepresentation by native genera

Family

Aliens in native genera

P valueObserved Expected Differencea

Aquifoliaceaeb 2 2 0 …Brassicaceae 4 1 � .007*Caryophyllaceaeb 1 3 � .11Chenopodiaceae 3 1 � .03Convolvulaceaeb 9 7 � .22Cuscutaceaeb 1 1 0 …Cyperaceaeb 15 16 � .47Euphorbiaceaeb 11 6 � .02Fabaceaeb 18 10 � .01*Gentianaceae 1 0 � .02Malvaceaeb 8 6 � .19Myrtaceaeb 4 6 � .25Phytolaccaceaeb 1 0 � .05Plantaginaceaeb 5 5 0 …Poaceaeb 37 41 � .25Portulacaceae 2 0 � .03Ranunculaceae 4 1 � .01*Rosaceae 7 1 � .00004*Solanaceaeb 12 15 � .18Verbenaceaeb 0 3 � .02

a A negative difference is predicted by Darwin’s hypothesis.b Family included enough naturalized species to potentially support Dar-

win’s naturalization hypothesis.

* Significantly more aliens than expected in native genera, using a se-

quential Bonferroni correction for multiple comparisons ( ).P ! .05

nificance of that difference in an analogous fashion. Thebinomial probability distribution assumes sampling withreplacement (constant a/f ), but because n was always smallrelative to a and f, violation of this assumption has neg-ligible effects on the P values (Mendenhall et al. 1990). Inassessing significance in each family, a sequential Bonfer-roni adjustment was employed to control for multiplecomparisons (Wright 1992).

In my analyses, I used Cronquist’s (1988) system ofclassification at the family level because it was used byMabberley (1998), and Mabberley (1998) provides one ofthe most comprehensive and reliable sources of speciesnumbers per family and genus. Cronquist’s system is basedon putative evolutionary relationships, and some of Cron-quist’s families are polyphyletic (Chase et al. 1993). Un-fortunately, there is currently no complete phylogeny ofthe flowering plants at the genus level, preventing truephylogenetic analyses of these data. Nevertheless, there isno reason to believe that comparisons of native versusalien congeners within families would be biased by usingCronquist’s system, as opposed to alternative plant-familysystems.

Comparing Early and Later Naturalized Species

As a second test of Darwin’s hypothesis, I compared earlynaturalized species (pre-1900) with later naturalized spe-cies (post-1930) to determine whether later naturalizedspecies were less likely to belong to early naturalized gen-era. I obtained dates of naturalization from Wagner et al.(1999) and Wester (1992), which allowed me to classifythe naturalized flora broadly into early and later natural-izations. My choice of pre-1900 as early and post-1930 aslater was arbitrary, but I chose a 30-yr gap between thegroups to help ensure that most of the early naturalizationshad spread widely before naturalization of the post-1930species. Species first recorded as naturalized between 1900and 1930 were excluded from these analyses. As a finalcomparison, I used only species that were presumed to beaccidental introductions (Wester 1992; Wagner et al. 1999).This allowed me to examine patterns of naturalization,absent the whims and preferences of humans.

Results

The null hypothesis is that the relative number of natu-ralizations belonging to native versus alien genera is pro-portional to the number of species available to invade innative versus alien genera (a/f as defined in “Methods”).A finding of significantly less naturalization in native gen-era would support Darwin’s hypothesis. Results were an-alyzed by plant family, and although there are 87 plant

families with native representatives in the Hawaiian Is-lands, some families had no naturalized species and couldnot be analyzed. Other families had too few naturalizedspecies (insufficient statistical power) to allow rejection ofthe null hypothesis, even if none of the naturalized specieshad belonged to native genera. A total of 13 families con-tained enough naturalized species to support (or reject)Darwin’s naturalization hypothesis statistically. Only oneof these 13 families (Verbenaceae) had statistically fewernaturalized representatives in native genera than expected( ), but after adjusting this P value for multipleP p .02comparisons, it was no longer significant ( ; tableP 1 .051). The remaining 12 out of 13 families failed to showstatistical support for Darwin’s hypotheses. An additionalseven families had enough naturalized species to support(or reject) statistically only the hypothesis that naturalizedspecies are more likely to belong to native genera (oppositeof Darwin’s hypothesis). When this opposing hypothesiswas evaluated, four of the 20 families had significantlymore naturalized species in native genera than expected,even after adjusting the P values for multiple comparisons(table 1). Disregarding probabilities and considering onlythe raw number of naturalized species belonging to native

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Notes and Comments 327

Table 3: Observed numbers of accidentally introducedpost-1930 naturalized species belonging to pre-1900genera versus expected numbers, by family

Observed Expected Differencea

Amaranthaceae 6 1 �Apiaceae 2 0 �Asteraceae 4 1 �Boraginaceae 0 0 0Brassicaceae 2 0 �Caryophyllaceae 0 2 �Chenopodiaceae 0 0 0Convolvulaceae 1 1 0Cyperaceae 3 0 �Euphorbiaceae 5 2 �Fabaceae 1 0 �Malvaceae 1 0 �Onagraceae 1 0 �Plantaginaceae 2 2 0Poaceae 0 0 0Polygonaceae 5 1 �Rubiaceae 0 0 0Solanaceae 3 2 �

Note: All families with two or more accidentally introduced nat-

uralized species are listed.a A negative difference is predicted by Darwin’s naturalization

hypothesis.

Table 2: Tests for significant underrepresentation (and over-representation) among all post-1930 naturalized species belong-ing to pre-1900 genera, grouped by family

Family Observed Expected Differencea P value

Amaranthaceae 3 1 � .03Apiaceae 2 0 � .01*Brassicaceae 3 1 � .02Cyperaceae 3 0 � .008*Euphorbiaceae 5 3 � .13Fabaceae 10 8 � .20Poaceae 16 9 � .007*Polygonaceae 7 1 � .0001*Rosaceae 6 1 � .001*Sapindacaeae 1 0 � .01*Solanaceae 6 5 � .33Verbenaceae 2 4 � .02

Note: Only families with a sufficient number of naturalized species to

potentially observe significant over- or underrepresentation are listed.a A negative difference is predicted by Darwin’s hypothesis.

* Significantly more post-1930 aliens belonging to pre-1900 genera than

expected, using a sequential Bonferroni correction for multiple comparisons

( ).P ! .05

genera, I found that 11 of the 20 families had more nat-uralized species in native genera than expected, while onlysix families had fewer naturalized species in native generathan expected (table 1).

Considering post-1930 invaders belonging to pre-1900genera, 12 families had a sufficient number of naturalizedspecies for analysis. One of the 12 families (Verbenaceae),seemed to support Darwin’s naturalization hypothesis( ), but again, this finding was not significantP p .02( ) after adjusting for multiple comparisons (tableP 1 .052). The remaining 11 out of 12 families provide no supportfor Darwin’s hypothesis. In fact, six of the 12 familiesprovided statistical support for the opposite of Darwin’shypothesis (later naturalizations were more likely to belongto the same genera than early naturalizations; table 2). Ifone considers only accidentally introduced species, thesmaller sample size provided reduced power for statisticaltesting, so families were simply classified as having moreor fewer post-1930 naturalizations from pre-1900 generathan expected (table 3). A nonparametric sign test wasthen used to determine whether there was a significantpattern. Among accidentally introduced post-1930 natu-ralizations, families were more likely to have an excess ofspecies belonging to pre-1900 genera than a deficit (signtest, ; table 3), again the opposite of Darwin’sP p .003naturalization hypotheses.

Discussion

Darwin (1859, p. 86) initially considered the possibilitythat aliens from native genera would be more likely to

naturalize: “It might have been expected that the plantswhich would succeed in becoming naturalized in any landwould generally have been closely allied to indigenes; forthese are commonly looked at as specially adapted for theirown country.” But after comparing raw numbers of speciesin native and alien genera, Darwin (1859) rejected thisidea in favor of the hypothesis that competition from spe-cies in native genera reduces naturalization by alien con-geners. Elton (1946) also noted that communities of nativespecies frequently contain only one species per genus, andlike Darwin, he implicated historical effects of competitionas the cause of this pattern. Williams (1947, 1951) lateridentified flaws in Elton’s (1946) analysis and came to theopposite conclusion: congeners are more likely to co-occurwithin many communities than expected by chance. In asimilar analysis comparing islands and mainlands, Sim-berloff (1970) concluded that species-genus ratios for mostisland biota did not differ from those expected based onrandom drawings of equal-sized biotas from a mainland;these results failed to support Grant’s (1966) hypothesisthat competition among congeners has led to reduced spe-cies-genus ratios on islands. In examining the insect faunasof Hawaii and North America, Simberloff (1986) alsofound no consistent relationship between the fraction ofnative versus naturalized insect fauna among insect orders,which also fails to support the hypothesis that biotic re-sistance has prevented insect naturalizations, at least at the

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328 The American Naturalist

level of orders. Recent findings of a positive associationbetween native-plant species richness and naturalized-plant species richness further open to question the generalimportance of biotic resistance in affecting plant natural-izations (Lonsdale 1999; Stohlgren et al. 1999).

Although observational studies based on species listscannot usually tell us what mechanism(s) is responsiblefor a pattern, such studies can be useful in stimulatinghypotheses and further tests. The naturalized flora of theHawaiian Islands are clearly consistent with Darwin’s orig-inal line of thinking; the indigenous flora has developedover at least 11 million years (Macdonald and Abbott1970) from a subset of arrivals that were capable of sur-viving in the Hawaiian environment. It should not besurprising that new, human-facilitated arrivals belongingto successful indigenous genera have a higher probabilityof succeeding. This would be especially true if the newarrivals were introduced into disturbed habitats with min-imal interaction with the native flora, diseases, andherbivores.

We might expect to see more support for Darwin’s nat-uralization hypothesis when we compare early versus laternaturalizations because naturalized species more oftengrow together in the same human-impacted habitats, lead-ing to greater potential for direct competition. Yet, evenamong early and later naturalized species, the pattern wasopposite to Darwin’s hypothesis: for many families, re-cently naturalized species were unexpectedly likely to be-long to the same genera as species that had naturalized30–250 yr earlier. Lockwood (1999) concluded that certainbird families and genera were preferred by humans (e.g.,for pets or game), making them more likely to be intro-duced. Human preferences for some plant genera couldalso be reflected in the naturalized plant flora of the Ha-waiian Islands. For example, new species of certain grassgenera that produce high-quality fodder (e.g., Eragrostis,Panicum, Paspalum) have been regularly introduced to theHawaiian Islands over the past 200 yr for agronomic pur-poses, increasing the likelihood of observing congenersamong old and recent naturalizations. Yet, the same pat-tern was found even among accidental introductions, in-dicating that human whims are not the sole source of thepattern. As with the indigenous flora, accidental natural-izations belong to a small subset of all introduced genera(Williamson 1996), and this subset of genera may haveecological characteristics that allowed them to succeed inHawaiian environments. Alternatively, the pattern amongaccidental introductions could be explained by certaingenera having a shared propensity for long-distance dis-persal (Simberloff 1970) or, more specifically, hitchhikingwith humans.

Another approach to testing Darwin’s hypothesis is toexamine extinction rates or failed naturalizations among

introductions. In examining bird naturalizations to Ha-waiian Islands, Moulton and Pimm (1986) failed to findevidence that species introduced to islands having estab-lished congeners were more likely to go extinct. Analysesof successful versus failed establishment of biocontrolagents may also lead to hypotheses about factors affectingnaturalization (Simberloff 1986). Ehler and Hall (1982)observed a negative relationship between establishmentrate among biocontrol agents and number of biocontrolagents released on a target. This pattern could have beendue to competition or other forms of biotic resistance likepredation, as documented by Goeden and Louda (1976)for a few biocontrol introductions. We know that somealien plant introductions have failed to become establishedin Hawaii based on single herbarium specimens collected50 yr ago or more (some examples are given in Wagneret al. 1999). Unfortunately, we do not have sufficient dataon failed introductions for the types of analyses that havebeen reported for birds and biocontrol agents.

Elton (1946) reported species-genus ratios ranging from1.06 to 1.45 for 25 native plant communities ranging fromthe Tropics to the Arctic. Although the current analysesexamined the flora of the Hawaiian Islands as a whole,congeners do appear to grow together more frequently inthe naturalized flora of the Hawaiian Islands than in thenative communities surveyed by Elton (1946). For ex-ample, the alien plant community of the dry, lowland Ha-waiian Islands (Whistler 1995) averages 1.82 species pergenus, outside the range reported by Elton (1946). Humandisturbance has possibly limited competitive exclusion(Wilson 1990), or alien communities may be too new(most aliens arrived within the past 250 yr) to experienceextinction within the multispecies genera. Of course thisreasoning is weak since persistent human disturbance isalso common in California, where aliens with native con-geners seem less likely to become naturalized (Rejmanek1998).

Conclusions

The importance of biotic resistance in preventing plantinvasions has been little studied (Mack 1996), but we canlook for circumstantial evidence in the form of a reducedprobability of naturalization by species with native con-geners (Darwin 1859). Although certain plant families inCalifornia and Australia have provided intriguing evidencein support of Darwin’s naturalization hypothesis (Rejma-nek 1998), results from the flora of the Hawaiian Islandsconflict with these findings. This leads to two alternativeinterpretations; either the results reported for a few fam-ilies by Rejmanek (1998) are anomalies or the compositionof communities in the Hawaiian Islands, and perhaps is-

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Notes and Comments 329

lands in general, are regulated by different factors thancontinental systems (reviewed by Simberloff 1970; Carl-quist 1974). Although competition between introducedand native congeners or early and later congeneric intro-ductions has often been proposed to affect species survivaland abundance (Diamond and Case 1986; Williamson1996), on average, the advantages of a close relationshipmay outweigh the drawbacks (Williams 1951).

Acknowledgments

I thank D. Simberloff and two anonymous reviewers forcomments and suggestions that improved this work.

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