Exotic snakes in São Paulo City, southeastern Brazil: why xenophobia?

Page 1

Biodiversity and Conservation 11: 327–339, 2002.© 2002 Kluwer Academic Publishers. Printed in the Netherlands.

Exotic snakes in São Paulo City, southeastern Brazil:why xenophobia?

ANDRÉ ETEROVIC1,2 and MARCELO RIBEIRO DUARTE1,3,∗1Laboratório de Herpetologia, Instituto Butantan, Avenida Vital Brazil 1500, CEP 05503-900, SãoPaulo; 2Laboratório de Ecologia Evolutiva, Departamento de Ecologia Geral, Instituto de Biociências,Universidade de São Paulo, Rua do Matão 321; 3Departamento de Zoologia, Instituto de Biociências,Universidade Estadual Paulista, Botucatu, SP, Brazil; *Author for correspondence (e-mail: [email protected])

Received 30 August 2000; accepted in revised form 2 April 2001

Abstract. Introduced exotic species cause environmental changes and threat public health in target sites.Illegal trade has enhanced this problem. To first report these risks in Brazil, exotic snakes found in SãoPaulo City (SPC) (23◦32′ S, 46◦38′ W), southeastern Brazil, and sent to Instituto Butantan between 1995and 2000, were listed and characterized by their biological attributes. Seventy-six individuals of sixteenalien species were collected. Euriecians snakes, mainly booids, were predominant. Using multivariate tech-niques, their ecological niches were compared to those of 26 native species, as a way to point out theresource’s availability. To evaluate the potential of successful implantation, two species absent in SPC andconsidered as problem snakes are included in these analyses: the brown treesnake Boiga irregularis and thehabu Trimeresurus flavoviridis. There were niche similarities between these pest snakes, exotic booids andnative viperids largely due to the similarities in the chosen prey (mammals), diel activity (nocturnal), colorpattern (variegated) and body size (medium to large). To avoid predictable undesirable effects of implantedpest snakes, traffic control and punishment should be improved, as well as parallel environmental educationprograms.

Key words: animal trade, biological conservation, Brazil, ecological niche, exotic species, snakes

Introduction

The major risks of human-induced introductions of exotic animals are: (1) popu-lation depletion by hunting in original countries (Dodd 1987, 1993; Adams et al.1994; Pough et al. 1998); (2) threats to public health by zoonoses, bites or envenoma-tion (Reid 1978; Minton 1996; Rodda et al. 1997); (3) introduction of new parasites(Reinert and Ruppert Jr 1999); and (4) changes in native fauna of target countries(Savidge 1987; Rodda and Fritts 1992; Martínez-Morales and Cuarón 1999). A crit-ical example of snake introduction is that of the brown treesnake Boiga irregularisin Guam. Like the habu Trimeresurus flavoviridis in some Japanese islands, it needscostly management strategies (Rodda et al. 1999b). The development of global com-munication and international market has enhanced this problem (Rodda et al. 1997):in a few minutes, one can find a long list of species for sale by Internet, many of which

Page 2

328

are regarded by CITES and IUCN as endangered. Both the introduction of exoticsnakes and the commerce of native species as pets have only recently received moreattention by environmental agencies in the USA (Smith and Kohler 1978; Adamset al. 1994; Pough et al. 1998; Duellman 1999). In Brazil, nothing has been publishedon this matter.

São Paulo City (SPC; 23◦32′ S, 46◦38′ W; 760 m above sea level), the capital ofSão Paulo State, is the main commercial center in southeastern Brazil. General trade,including that of exotic pet snakes, is concentrated in this part of the country. Illegaltraffic exists, as evidenced by recent IBAMA (the National Agency for Environment)apprehensions. Despite the prohibition of importing exotic snakes and of trading na-tive ones (Federal Order no. 93/98, 7 July 1998), they are still found as pets in SPC.The illegal status leads to an absence of specialist’s care and the pet snakes frequentlysuffer from sick or undesirable conditions. Therefore, their owners (or ‘parents’) oftenrelease them in many parts of the city, where they also go when they escape. Theseareas are subject to different degrees of anthropic activities and they house at least26 native snake species (Puorto et al. 1991). When recaptured, the destination ofsuch alien snakes is frequently the Instituto Butantan (IB), a traditional ophiologycenter in SPC. Received individuals are exposed to public visiting at IBs museumand, after their death, they are incorporated into the Alphonse Hoge’s HerpetologicalCollection. This procedure is also applied to thousands of native specimens that arriveat IB yearly, sent by occasional collectors from all Brazilian regions, as well as byother public institutions (including IBAMA).

This paper is the first quantitative survey of exotic snakes’ arrivals at IB, presentedas a measure of the colonization risk of SPC and, by extent, of preservation areas inBrazil. A discussion concerning the conservation aspects of snake introduction is alsomade based on a qualitative approach of the ecological niche.

Methods

A checklist of native species by Puorto et al. (1991) based on individuals sent to IB in1988–1989 was assumed to reflect the actual composition of the snake community atSPC. The majority of exotic snakes found in SPC and sent to IB from January 1995 toApril 2000 were identified to species level. Translocated species and subspecies, i.e.species and subspecies that occur naturally in Brazil but not in SPC, were consideredas exotic. The number of individuals in each taxon was recorded. To show the patternof new species arrivals, a collector’s curve was designed by Sanders’ RarefactionMethod (Hurlbert 1971; Ludwig and Reynolds 1988). It consists of re-sampling withreplacement (90 times, in this case) blocks of a variable number of individuals fromthe original data set and subsequent fitting of a logarithmic expression.

Both exotic and native snakes were qualitatively classified (presence/absence)by 24 biological categories concerning reproductive mode, prey type, foraging mode,

Page 3

329

Table 1. Biological categories used in a qualitative classification of the ecological nicheof exotic and native snake species found in SPC, Brazil.

Code Category Description

ovi Oviparity Reproductive modeviv Viviparity Reproductive modemam Mammals Frequent use of this preybir Birds Frequent use of this preyliz Lizards Frequent use of this preysna Snakes (including amphisbaenians Frequent use of this prey

and caecilians)anu Anurans Frequent use of this preyfis Fishes Frequent use of this preyinv Invertebrates Frequent use of this preyact Active search Foraging modesit Sit and wait Foraging modeter Terrestrial Frequent use of the ground surfacearb Arboreal Frequent use of treesacq Aquatic Frequent activity in waterfos Fossorial (and criptozooic) Frequent activity under the groundvar Variegated Color patternsmo Smooth (uniform coloration) Color patternred Red (mainly in annuli) Color patternstr Longitudinally striped Color patternsma Small-sized Average body length (< 0.5 m)med Medium-sized Average body length (0.5–1.5 m)big Large-sized Average body length (> 1.5 m)diu Diurnal Frequent activity in this periodnoc Nocturnal Frequent activity in this period

habitat use, color pattern, body size and circadian activity of adults (Table 1). Onto-genetic changes were not considered. Data were obtained by published references orpersonal observations. In few cases when data were not available, attributes were in-ferred by that of closely related congeneric species. All of the employed attributes aredependent on environmental conditions and resources that satisfy the requirements ofeach species, i.e. they are linked to the n-dimensional hypervolumetric Hutchinson’secological niche (Reinert 1993; Begon et al. 1996; Ricklefs 1996). Based on thisstatement, these multivariate data were used to describe qualitatively the niche ofeach snake. The categories ‘oviparity’, ‘active search’, ‘terrestrial’, ‘medium-sized’and ‘diurnal’ were presented by the majority of the snakes studied here, and theywere used as default. In other words, the remaining categories were considered as‘deviations’ from such ‘main patterns’, contributing to enhance differences betweenecological niche of the snakes in further analyses.

To estimate niche similarities, the taxon-categories matrix was subjected to clus-tering analysis (e.g. Duellman 1978, Martins and Oliveira 1998), using Jaccard’ssimilarity index and UPGMA method (Ludwig and Reynolds 1988; Magurran 1988).A correspondence analysis (Gauch 1982; Ter Braak 1986, 1988; Ludwig and

Page 4

330

Reynolds 1988) allowed an ordination of the species by the same attributes. As thesemultivariate methods were employed in an exploratory way, statistical tests were notapplied (Ter Braak 1986, 1988). Two pests snakes not found in SPC were included inthese analyses, as model parameters of successfully implanted species: the colubridB. irregularis and the viperid T. flavoviridis. The brown treesnake is a big variegatedsnake, oviparous, mainly arboreal and nocturnal, that searches actively for rodents,birds, lizards and anurans (Rodda et al. 1999a). The habu has the same attributes,but it is less arboreal than B. irregularis and it preys mainly on rodents and birds byambushing (Mishima et al. 1999).

Results

Twenty-six species of native snakes found in SPC are listed in Table 2. Seventy-sixindividuals of sixteen exotic species found in SPC were sent to IB from January 1995to April 2000. The yearly capture reaches its maximum value (32 snakes, 42% of to-tal) in 1999, due to one of IBAMAs apprehensions of 22 illegally captive individuals(Figure 1a). The collector’s curve and parameters of the fitted equation are presentedin Figure 1b. Fifty percent of the alien individuals found were from other areas ofSouth America, 22% from North America, 17% from Africa, 5% from Asia, 1% fromOceania, whereas the origins of the remaining 4% were not determined (Table 3).Booids (Boa constrictor, Corallus caninus, Epicrates cenchria, Liasis albertisi andPython spp.) represented 67% of total individuals, and the remaining were colubrids.The order of abundance of genera was: Boa (one species, three subspecies, 25% ofthe individuals), Python (three species, 22%), Lampropeltis (two species, 13%), Epi-crates (one species, four subspecies, 12%), Elaphe (two species, 8%), Corallus (onespecies, 7%), Boaedon (one species, 4%), Philodryas (one species, 4%), Lystrophis(two species, 3%), Liasis (one species, 1%) and Thamnophis (one species, 1%).

Cluster analysis of interspecific similarities in biological attributes of native andexotic species (Tables 2 and 3) revealed three main groups, at 0.2 similarity level(Figure 2). Group 1 has 5 native and 10 exotic species. It includes all booids, both ab-origine viperids (Bothrops jararaca and Crotalus durissus), both pseudoboines (Oxy-rhopus spp.), and other medium-sized colubrids (Boaedon fuliginosus, Elaphe spp.,Tropidodryas striaticeps). Both problem snakes, B. irregularis and T. flavoviridis,also compound this group. All of the Group 1 species feed mainly on mammals.Group 2 has three native (the elapid Micrurus corallinus, and the colubrids Apos-tolepis assimilis and Erythrolamprus aesculapii) and three exotic snakes (Philodryaspsammophideus, and Lampropeltis spp.), that prey on serpentiform animals. Group3 included 18 native and three exotic snakes (Lystrophis dorbignyi, L. semicinctusand Thamnophis sirtalis), all being medium and small colubrids that prey mainly onanurans or invertebrates (the case of Atractus reticulatus, Liotyphlops beui, Sibyno-morphus mikanii, Tantilla melanocephala and Tomodon dorsatus). Rising the level

Page 5

331

Table 2. Native snakes found in SPC, Brazil. This checklist was based on 309individuals sent to IB in 1989–1990 (Puorto et al. 1991). Biological categoriesused to define the qualitative ecological niche of each species were coded as inTable1. The categories ‘ovi’, ‘act’, ‘ter’, ‘med’ and ‘diu’ were omitted. Referen-ces are: (D) Duellman 1978; (G) Greene 1997; (J) Jordão and Bizerra 1996; (L)Leynaud and Bucher 1999; (M) Marques 1998; (Ma) Martins and Oliveira 1998;(S) Sazima and Haddad 1992; (V) Vitt and Vangilder 1983. Asterisks indicateinferences based on attributes of congeneric species.

Species Categories (References)

Apostolepis assimilis (Reinhardt 1861) sna/fos/red/sma/noc (G)Atractus reticulatus (Boulenger 1885) inv/fos/smo/sma/noc (D∗/L∗)Bothrops jararaca (Wied 1824) viv/mam/sit/var/noc (M/S)Chironius bicarinatus (Wied 1820) anu/arb/smo (M/S)Crotalus durissus (L. 1758) viv/mam/sit/var/noc (S/V)Echinantera undulata (Wied 1824) anu/smo/sma (M)Erythrolamprus aesculapii (L. 1766) sna/red (D/M/Ma/S)Helicops modestus (Günther 1861) viv/anu/fis/acq/smo/noc (M∗)Liophis almadensis (Wagler 1824) anu/acq/var/red/sma (L)L. jaegeri (Günther 1858) anu/smo/sma (L)L. miliaris (L. 1758) anu/fis/acq/smo/noc (M/S)L. poecylogyrus (Wied 1825) anu/smo/sma/noc (D/L/V)Liotyphlops beui (Amaral 1924) inv/fos/smo/sma (L∗)Micrurus corallinus (Merrem 1820) sna/fos/red (M)Oxyrhopus clathratus (Dumeril, mam/red/noc (M)

Bribon and Dumeril 1854)O. guibei (Hoge and Romano 1976) mam/red/noc (S)Philodryas olfersi (Lichtenstein 1823) mam/bir/anu/arb/smo (S/V)P. patagoniensis (Girard 1857) mam/sna/anu/smo (S)Sibynomorphus mikani (Schlegel 1837) inv/var/sma/noc (L∗/M∗)Simophis rhinostoma (Schlegel 1837) anu/red/sma (J)Tantilla melanocephala (L. 1758) inv/fos/smo/sma/noc (D/Ma)Thamnodynastes strigatus (Günther 1858) viv/anu/smo/noc (M)Tomodon dorsatus (Dumeril and Bribon 1853) viv/inv/smo (M)Tropidodryas striaticeps (Cope 1870) mam/arb/var (M∗)Waglerophis merremi (Wagler 1824) anu/var/smo (V)Xenodon neuwiedii (Günther 1863) anu/var (M/S)

of clustering up to 0.4, the greatest group (1′) included the two pests, the majority ofbooids and the native viperids, all of which are variegated and nocturnal snakes.

In the correspondence analysis (Figure 3), the first (horizontal) axis (eigenvalue =0.57; variance of species data = 18.6) seems to be inversely correlated to body size:small snakes, such as L. beui and T. melanocephala, are on the right side, opposedto the boas and pythons. In relation to the second (vertical) axis (eigenvalue = 0.48;variance of species data = 15.8), several prey specialists, such as the serpentiform-prey-eaters (top) and the invertebrate-eaters (bottom, e.g. the malacophagous T. dors-atus), were located far from the origin, where snakes that prey on mammals, birdsand anurans were located. Again, booids appear close to the native viperids and thetwo pest snakes. It is important to point out that ‘body size’ and ‘prey type’ are not

Page 6

332

Figure 1. Patterns in arrivals of exotic snakes at IB. (a) Number of exotic snakes (n = 76) found in SPC,Brazil, and sent to IB from January 1995 to April 2000. (b) Collector’s curve of exotic snakes found inSPC and sent to IB from 1995 to 2000. Data on increasing number of individuals were created by Sanders’Rarefaction Method, i.e. re-sampling with replacement (90 times) from the original data set (n = 76individuals; S = 16 species).

‘true variables’ in the sense of the analysis described above, as is the case of the cate-gories ‘small sized’, ‘large sized’, ‘mammals’, ‘birds’, ‘lizards’, ‘snakes’, ‘anurans’,‘fishes’, and ‘invertebrates’. The location of each category in the ordination diagram(Figure 3, left graph) indicates their relative importance to explain the variance of thespecies data (Ter Braak 1986, 1988).

Discussion

No evidence of successful colonization by alien snakes, i.e. settlement of a repro-ductive population, was obtained until now in SPC. However, the risk of reaching aMinimun Viable Population (as presented in Dodd 1993) was assumed to be in directcorrelation to some factors:

1. Number of individuals actually presented in the city.2. Chance of accessing ‘outdoor environments’, by escaping (accidental) or releas-

ing (intentional). It largely depends on the type of management in captivity (sci-entific institutions, legal pet shops, illegal traffic, house of aficionados).

3. Individual reproductive condition (sex, age and probability of outdoor mating,ability to store sperm, existence of parthenogenesis).

4. Demographic parameters under phylogenetic constrains (age of maturation, clu-tch size, number of reproductive events, lifespan).

5. Specific niche and environmental constrains (e.g. abiotic variables, food avail-ability, predation, competition, diseases).

It is out of scope of the present paper to make a detailed evaluation of the factors2, 3 and 4, because no data are available for all the species. A risk assessment wasdone strictly based on the following statements:

(i) Individuals of exotic species were actually present in SPC.

Page 7

333

Tabl

e3.

Exo

ticsn

akes

foun

din

SPC

,Bra

zil.

nde

note

sth

enu

mbe

rof

indi

vidu

als

ofa

give

nsp

ecie

s(t

otal

n=

76)

sent

toIB

from

Janu

ary

1995

toA

pril

2000

.B

iolo

gica

lca

tego

ries

used

tode

fine

the

qual

itativ

eec

olog

ical

nich

eof

each

spec

ies

wer

eco

ded

asin

Tabl

e1.

The

cate

gori

es‘o

vi’,

‘act

’,‘t

er’,

‘med

’an

d‘d

iu’

wer

eom

itted

.R

efer

ence

sar

e:(C

)C

obor

n19

91;

(D)

Due

llman

1978

;(G

)G

reen

e19

97;

(L)

Ley

naud

and

Buc

her

1999

;(M

a)M

artin

san

dO

livei

ra19

98;(

Mu)

Mur

phy

and

Hen

ders

on19

97;(

R)

Ros

sman

etal

.199

6;(T

)Te

nnan

t198

4;(V

)V

ittan

dV

angi

lder

1983

.Ast

eris

ksin

dica

tein

fere

nces

base

don

attr

ibut

esof

cong

ener

icsp

ecie

s.

Spec

ies

Ori

gin

Attr

ibut

es(R

efer

ence

s)n

Boa

cons

tric

tor

(L.1

758)

Mex

ico

toA

rgen

tina,

Ant

illes

viv/

mam

/bir

/arb

/var

/big

/noc

(D/M

a/V

)19

a

Boa

edon

fuli

gino

sus

(Boi

e18

27)

Afr

ica

(SSa

hara

excl

udin

gfo

rest

s)m

am/s

mo/

noc

(C)

3C

oral

lus

cani

nus

(L.1

758)

Am

azon

ian

Bas

invi

v/m

am/s

it/ar

b/va

r/bi

g/no

c(D

/Ma)

5E

laph

egu

ttat

a(L

.176

6)C

USA

toM

exic

om

am/v

ar(T

)3

Ela

phe

obso

leta

(Say

1823

)E

USA

toN

EM

exic

om

am/a

rb/v

ar/s

mo/

str

(T)

1E

picr

ates

cenc

hria

(L.1

758)

Am

azon

asto

Arg

entin

aan

dPa

ragu

ayvi

v/m

am/b

ir/a

rb/v

ar/b

ig/n

oc(D

/Ma/

V)

9b

Lam

prop

elti

sge

tulu

s(L

.176

6)U

SA(c

oast

toco

ast)

mam

/bir

/liz/

sna/

var/

red

(T)

7c

Lam

prop

elti

str

iang

ulum

(Lac

eped

e17

89)

Can

dE

USA

toC

Am

eric

a,m

am/b

ir/li

z/sn

a/va

r/re

d(G

)1

NW

Col

ombi

aan

dE

cuad

orL

iasi

sal

bert

isiP

eter

s&

Dor

ia18

78N

ewG

uine

a,A

ustr

alia

nIs

land

sm

am/a

rb/s

mo/

big/

noc

(C)

1Ly

stro

phis

dorb

igny

iSE

Bra

zilt

oA

rgen

tina

anu/

var/

red/

sma

(L)

1(D

umer

il,B

ribo

n&

Dum

eril

1854

)Ly

stro

phis

sem

icin

ctus

SWB

razi

l,S

Bol

ivia

,an

u/va

r/re

d/sm

a(L

∗ )1

(Dum

eril,

Bri

bon

&D

umer

il18

54)

Can

dN

Arg

entin

a,N

Para

guay

Phi

lodr

yas

psam

mop

hide

usG

ünth

er18

72E

Bol

ivia

,SW

Bra

zilt

oA

rgen

tina

and

Uru

guay

liz/s

na/s

tr(L

)2

Pyt

hon

mol

urus

(L.1

758)

Indi

a,In

do-C

hina

,SC

hina

,Mal

ayan

Isla

nds

mam

/bir

/acq

/var

/big

/noc

(Mu)

4d

Pyt

hon

regi

us(S

haw

1802

)W

and

CA

fric

am

am/a

rb/v

ar/b

ig/n

oc(M

u∗)

8P

ytho

nse

bae

(Gm

elin

1789

)A

fric

a(S

Saha

ra)

mam

/bir

/acq

/var

/big

/noc

(Mu)

2T

ham

noph

issi

rtal

is(L

.176

6)S

Can

ada

and

USA

(coa

stto

coas

t)vi

v/an

u/fis

/inv/

acq/

str

(R)

1E

laph

esp

.und

eter

min

ed2

Lam

prop

elti

ssp

.und

eter

min

ed2

Phi

lodr

yas

sp.u

ndet

erm

ined

1P

ytho

nsp

.und

eter

min

ed3

aIn

divi

dual

sar

e5

B.c

.am

aral

i,11

B.c

.con

stri

ctor

,1

B.c

.occ

iden

tali

san

d2

unde

term

ined

subs

peci

es.

Onl

yth

edi

stri

butio

nof

B.c

.am

aral

ire

ache

sSã

oPa

ulo

stat

e.b

4E

.c.a

lvar

ezi,

2E

.c.a

ssiz

i,2

E.c

.cra

ssus

and

1E

.c.h

ygro

phil

us.O

nly

the

dist

ribu

tion

ofE

.c.c

rass

usre

ache

sSã

oPa

ulo

stat

e.c

5L

.g.c

alif

orni

ae,1

L.g

.nig

ritu

san

d1

unde

term

ined

subs

peci

es.

d3

P.m

.biv

itta

tus

and

1un

dete

rmin

edsu

bspe

cies

.

Page 8

334

Figure 2. Dendrogram from clustering analysis (Jaccard similarity index, UPGMA, cofenetic index =0.826) of snakes found in SPC, based on qualitative biological attributes. Asterisks indicate exotic species.Boiga irregularis and T. flavoviridis (in boxes) were not found in SPC but are problem species in PacificIslands (see text).

(ii) There were (qualitative) niche similarities between alien and native snakes.(iii) There were (qualitative) niche similarities between these alien snakes and two

other species considered as pests elsewhere.

Page 9

335

Figure 3. Results of the correspondence analysis of snakes found in SPC, based on qualitative biologicalattributes. Left plot shows score for each of the biological categories as coded in Table 1. Right plot showsscore for each of the 26 native species (Table 2) as indicated by a three-character code (the first letter of thegenus plus the two first letters of species name; except for Thamnodynastes strigatus (tha) and T. striaticeps(tro) and that for each of the 16 exotic species (Table 3) by a four-character code (the first letter of the genusplus the three first letters of the species name). Boiga irregularis (birr) and T. flavoviridis (tfla) were notfound in SPC but are problem species in Pacific Islands (see text). Horizontal (eigenvalue = 0.57) andvertical (eigenvalue = 0.48) axes represent 34.4% variance of species data (total inertia = 3.07).

The sample of exotic snakes sent to IB is an underestimate of ‘who’ and ‘howmany’ are released in SPC and, therefore, is an underestimate of alien introductionin Brazil. Note that exotic living individuals in scientific collections were consid-ered here ‘with no risk’ of escaping from captivity or being released (see ‘factor 2’above), and were not included in this discussion. Using a reasonable extrapolationof the adjusted collector’s curve in Figure 1b, one can estimate 20 accumulated spe-cies (77% of the present native richness, an increase of 25% in the ‘exotic richness’)when the number of exotic snakes reaches 182 individuals. This scenario of four newexotic species arriving at SPC, besides those 16 reported here, could be expectedfor the year 2008 if both (1) the present average arrival of 14.3 individuals/year and(2) the dominance pattern of ‘captured alien community’ are fixed. At least the firstassumption was not supported by the annual capture plot in Figure 1a: no significanttendency was evident (y = 2.47 + 3.20x; R2 = 0.31; P > 0.05). Moreover, thesecond assumption is linked to oscillations of international trade and to the chanceof importing new species, legally or not. Therefore, arrivals of exotic snakes at anyplace should be considered primarily a stochastic, unpredictable event.

Page 10

336

The different conditions under which each individual was captured restrict thedirect correlation between the number of species effectives and the chance of coloni-zation. However, it constitutes a reasonable (and available) first approach. Out of theexotic snakes analyzed, booids composed the majority of the sample. These eurie-cians snakes have an extreme ability of adaptation in many ecotopes (as in Martínez-Morales and Cuarón 1999). The same could possibly be true of Lampropeltisand Elaphe species, which show broad geographical distributions (Coborn 1991).

There is an example of an established population of B. constrictor in CozumelIsland (Martínez-Morales and Cuarón 1999), the first snake in the SPCs exotic abun-dance rank (19 individuals, see Table 3). Besides ecological factors, phylogeny alsocontributes to natural history patterns (as in Martins and Oliveira 1998), resultingin niche similarities between closely related species. Therefore, once Elaphe taeni-ura was introduced to Ryukyu Archipelago (Ota 1999), the presence of congenericspecies in SPC also needs attention.

The performed multivariate exploratory analysis shows ‘where’, in a multidimen-sional space among the native snakes, the exotic snakes have their potential niche. Asan example, the booids would be found ‘somewhere’ near the viperids but far fromL. beui and T. melanocephala, the invertebrate-eaters, fossorial, small-sized snakes.No assumptions on competition or predation involving exotic and native species weredone. The similarities found by these analysis only indicate a chance that alien spe-cies would find in SPC some conditions that correspond to their needs. Additions ofB. irregularis and T. flavoviridis to the analyses allowed a comparison with effectivecolonizers. Therefore, niche similarities between these two snakes and the booids in-dicate that boas and pythons may be as successful as the known pest snakes, probablyusing the same type of resources available to the native pitvipers.

The introduction of B. irregularis to Guam is largely reputed as a factor that con-tributed to depress the local avifauna (Savidge 1987). On the other hand, T. flavo-viridis is native from Japanese Islands (despite the possible human introduction toMinnajima) (Katsuren et al. 1999), reaching high population densities but with noecological damage attributed to them. However, due to the risk of bites, substantialefforts to reduce those populations have been made. This measure itself (removal ofa top predator) may affect the food chain.

Quantitative research on the intensity of resource exploitation and environmentalrequirements by both native and exotic species (not only snakes) are needed to allowmore robust comparisons between habitat use (Vitt 1987; Reinert 1993), as well asbetween niches. While this knowledge is not a current device, a little bit of xenopho-bia is a salutary prophylactic way to prevent drastic changes in local communities byintroduced fauna (but see Smith and Kohler 1978 for alternative views).

Importing, keeping and commercializing dangerous or even poisonous snakes leadto a new public health problem (Reid 1978; Minton 1996). Some opistogliphodontand agliphodont snakes also present toxic secretions from Duvernoy’s glands (e.g.Philodryas, Assakura et al. 1992). No antiserum for alien species is available for the

Page 11

337

general public in SPC. Great constrictors, 67% of the present findings, can also causehuman death (Branch and Hacke 1980; Chiszar et al. 1993).

As pointed out by Fritts and Rodda (1999), some biological features of snakesrequire management strategies distinct from those applied to other vertebrates. Theyare well-hidden predators, with the absence of legs and elongation of body contribut-ing both to locomotion and to crypsis. They forage infrequently, and are able to storesperm for a long period. Because of this, snakes are generally difficult to capture,and their population sizes are difficult to assess, making it difficult to eradicate them,once they are established as a result of accidental (or intentional) transportation.

Management programs of introduced snakes may employ many public resources(Rodda et al. 1999b). As many researchers commonly suggest eradication of estab-lished populations of exotic snakes (Rodda and Fritts 1992; Katsuren et al. 1999;Martínez-Morales and Cuarón 1999), the exotic trade prohibition in Brazil has tobe sustained. Improved control and punishment may restrict illegal traffic only withparallel implementation of environmental education programs. Therefore, preventivemeasures should be preferred to corrective ones.

Acknowledgements

Thanks to our colleagues in IB Francisco L Franco, Hebert Ferrarezzi, and OtavioAV Marques for taxonomic and biological information; Amauri F da Silva, Circe Cde Albuquerque and Giuseppe Puorto for making records on exotic species undertheir responsibility available to us. OAVM, Cristiano C Nogueira, Leila L Longo,and Paula H Valdujo (IBUSP) read the drafts. Pérsio S Santos-Filho (IBUSP) madeimportant suggestions.

References

Adams CE, Thomas JK, Strnadel KJ and Jester SL (1994) Texas rattlesnake roundups: implications ofunregulated commercial use of wildlife. Wildlife Society Bulletin 22: 324–330

Assakura MT, Salomão MG, Puorto G and Mandelbaum FR (1992) Hemorragic, fibrinogenolytic andedema-forming activities of the venom of the colubrid snake Philodryas olfersii (green snake). Toxicon30: 427–438

Begon M, Harper JL and Townsend CR (1996) Ecology, 3rd Edition. Blackwell Science, Oxfordter Braak CJF (1986) Canonical correspondence analysis: a new eigenvector technique for multivariate

direct gradient analysis. Ecology 67: 1167–79ter Braak CJF (1988) CANOCO – a FORTRAN Program for Canonical Community Ordination by (par-

tial) (detrended) (canonical) Correspondence Analysis, Principal Components Analysis and RedundancyAnalysis (version 2.1). Groep Landbouwwiskunde, Wageningen

Branch WR and Hacke D (1980) A fattal attack on a young boy by an african rock python, Python sebae.Journal of Herpetology 14: 305–307

Chiszar D, Smith HM, Petkus A and Dougherty J (1993) A fattal attack on a teenage boy by a captive Bur-mese python (Python molurus bivitattus) in Colorado. Bulletin of the Chicago Herpetological Society28: 261–262

Coborn J (1991) The Atlas of Snakes of the World. TFH Publications, Neptune City

Page 12

338

Dodd Jr CK (1987) Status, conservation and management. In: Seigel RA, Collins JT and Novak SS (eds)Snakes: Ecology and Evolutionary Biology. Macmillan Publishing Company, New York

Dodd Jr CK (1993) Strategies for snake conservation. In: Seigel RA and Collins JT (eds) Snakes: Ecologyand Behavior, pp 363–393. McGraw Hill, New York

Duellman WE (1978) The biology of an equatorial herpetofauna in Amazonian Ecuador. The Universityof Kansas Museum of Natural Hystory Miscellaneous Publication 65: 1–352

Duellman WE (1999) Perils of permits: procedures and pitfalls. Herpetological Review 30: 12–16Fritts TH and Rodda GH (1999) Contributions of brown treesnakes and habu to science and society. In:

Rodda GH, Sawai Y, Chiszar D and Tanaka H (eds) Problem Snake Management, (Epilogue) pp 481–485. Comstock Publishing Associates, Ithaca

Gauch HG (1982) Multivariate Analysis in Community Ecology. Cambridge University Press, New YorkGreene HW (1997) Snakes: The Evolution of Mistery in Nature. University of California Press, Los

AngelesHurlbert SH (1971) The nonconcept of species diversity: a critique and alternative parameters. Ecology

52: 577–586Jordão RS and Bizerra AF (1996) Reprodução, dimorfismo sexual e atividade de Simophis rhinostoma

(Serpentes, Colubridae). Revista Brasileira de Biologia 56: 507–512Katsuren S, Yoshida C and Nishimura M (1999) A ten-year trapping program to eradicate Habu (Tri-

meresurus flavoviridis) from Minnajima, a small island in the Okinawa Islands, Japan. In: Rodda GH,Sawai Y, Chiszar D and Tanaka H (eds) Problem Snake Management, pp 340–347. Comstock PublishingAssociates, Ithaca

Leynaud GC and Bucher EH (1999) La fauna de serpientes del chaco sudamericano: diversidad, distrib-uicion geografica y estado de conservacion. Academia Nacional de Ciencias de Cordoba, Argentina,Miscelanea 98: 3–46

Ludwig JA and Reynolds JF (1988) Statistical Ecology: A Primer on Methods and Computing. John Wileyand Sons, New York

Magurran A (1988) Ecological Diversity and its Measurement. Princeton University Press, New JerseyMarques OAVM (1998) Composição faunística, história natural e ecologia de serpentes da Mata Atlântica,

na região da Estação Ecológica Juréia-Itatins, São Paulo, SP. PhD thesis, Universidade de São PauloMartínez-Morales MA and Cuarón AD (1999) Boa constrictor, an introduced predator threatening the

endemic fauna on Cozumel Island, Mexico. Biodiversity and Conservation 8: 957–963Martins M and Oliveira ME (1998) Natural history of snakes in forests of the Manaus region, Central

Amazonia, Brazil. Herpetological Natural History 6: 78–150Minton SA (1996) Bites by non-native venomous snakes in the United States. Wilderness and Environ-

mental Medicine 4: 297–303Mishima S, Tanaka H and Saway Y (1999) The biology of the Habu (Trimeresurus flavoviridis). In: Rodda

GH, Sawai Y, Chiszar D and Tanaka H (eds) Problem Snake Management, pp 29–43. Comstock Pub-lishing Associates, Ithaca

Murphy JC and Henderson RW (1997) Tales of Giant Snakes: A Historical Natural History of Anacondasand Pythons. Krieger Publishing Company, Malabar

Ota H (1999) Introduced amphibians and reptiles of the Ryukyu Archipelago, Japan. In: Rodda GH,Sawai Y, Chiszar D and Tanaka H (eds) Problem Snake Management, pp 439–452. Comstock PublishingAssociates, Ithaca

Pough FH, Andrews RM, Cadle JE, Crump ML, Savitsky AH and Wells KD (1998) Herpetology. Prentice-Hall, New Jersey

Puorto G, Laporta-Ferreira IL and Sazima I (1991) Serpentes na selva de pedra. Ciência Hoje 13:66–67

Reid HA (1978) Bites by foreign venomous snakes in Britain. British Medical Journal 1: 1598–1600Reinert HK (1993) Habitat selection in snakes. In: Seigel RA and Collins JT (eds) Snakes: Ecology and

Behavior, pp 201–240. McGraw Hill, New YorkReinert HK and Ruppert Jr RR (1999) Impacts of translocation on behavior and survival of Timber rattle-

snakes, Crotalus horridus. Journal of Herpetology 33: 45–61Ricklefs RE (1996) Ecology, 3rd Edition. WH Freeman and Company, New York

Page 13

339

Rodda GH and Fritts TH (1992) The impact of introduction of the colubrid snake Boiga irregularis onGuam’s lizards. Journal of Herpetology 26: 166–174

Rodda GH, Fritts TH and Chiszar D (1997) The disappearance of Guam’s wildlife. BioScience 47: 565–574

Rodda GH, Fritts TH, McCoid MJ and Campbell III EW (1999a) An overview of the biology of thebrown treesnake (Boiga irregularis), a costly introduced pest on Pacific Islands. In: Rodda GH, Sawai Y,Chiszar D and Tanaka H (eds) Problem Snake Management, pp 44–80. Comstock Publishing Associates,Ithaca

Rodda GH, Sawai Y, Chiszar D and Tanaka H (1999b) Snake management. In: Rodda GH, Sawai Y,Chiszar D and Tanaka H (eds) Problem Snake Management, pp 1–23. Comstock Publishing Associates,Ithaca

Rossman DA, Ford NB and Seigel RA (1996) The Garter Snakes: Evolution and Ecology. University ofOklahoma, Norman

Savidge JA (1987) Extinction of an island forest avifauna by an introduced snake. Ecology 68: 660–668Sazima I and Haddad CFB (1992) Répteis da Serra do Japi: notas sobre história natural. In: Morellato LPC

(org) História natural da Serra do Japi. Unicamp/Fapesp, CampinasSmith HM and Kohler AJ (1978) A survey of herpetological introductions in the United States and Canada.

Transactions of the Kansas Academy of Science 80: 1–24Tennant A (1984) The Snakes of Texas. Texas Monthly Press, AustinVitt LJ (1987) Communities. In: Seigel RA, Collins JT and Novak SS (eds) Snakes: Ecology and Evolu-

tionary Biology. Macmillan Publishing Company, New YorkVitt LJ and Vangilder LD (1983) Ecology of a snake community in Northeastern Brazil. Amphibia-Reptilia

4: 273–296

Page 14