limbata ( V a l e n c i e n n e s , 1 8 3 3 ) i n s o u t ...

R E G U L A R P A P E R

Population expansion of the invasive Pomacentridae Chromis

limbata (Valenciennes, 1833) in southern Brazilian coast:

long-term monitoring, fundamental niche availability and new

records

Antônio B. Anderson 1,2 | Jodir Pereira da Silva3 | Raquel Sorvilo3 |

Carlo Leopoldo B. Francini 4 | Sergio R. Floeter2 | Jo~ ao P. Barreiros5,6,7

1 Department of Oceanography, ICTIOLAB - Laboratory of Ichthyology, Federal University of Espírito Santo, Vitória, Espírito Santo , Brazil

2 Marine Macroecology and Biog eography Laboratory, Department of Ecolo gy and Zoology, Federal University of Santa Catarina, Florianópolis, Brazil

3 Departamento de Ciências, Colégio Técnico de Campinas (CTC), Universidade Estadual de Campinas (UNICAMP), Jorge de Figueiredo Corrêa , Campi nas, S~ ao Paulo,

Brazil

4 Instituto Laje Viva, S~ ao Pau lo, Brazil

5 Centre for Ecolog y, Evolution and Environmenta l Cha nges (CE3 C)/Azorean Biodiversity Group and 7, Universidade dos Açores Faculdade de Ciênci as Agrári as e–

do Ambiente , Angra do Heroísmo, Portugal

6 Faculdade de Ciências Agrárias e do Ambiente, University of Azores, R. da M~ ae de Deus, Ponta Delgada, Azores, Portugal

7 Programa de Pós-Gra duaç~ ao - Centro APTA Pescado Marinho, Instituto de Pesca, Avenida Francis co Matar azzo, 455 - Parque da Agua Branca - Barra Funda, Santos,

S~ ao Pau lo, Brazil

Correspondence

Antônio B. Anderso n, Laborat ory of

Ichthyology, Department of Oceanography,

Federal University of Espírito Santo, Vitória, ES 29075-910, Brazil/ Sergio R. Floeter, Marine

Macroecology and Biogeography Laboratory -

Federal University of Santa Catarina ,

Florianópolis, Santa Catarina - Brazil

Email: [email protected];[email protected]

Funding information

CNPq, Grant/Award Number: CNPq 475367/2006-5; ECOPERE-SE Project;

FAPES, Grant/Award Number: PROFIX

program Nº 10/2018 - T.O.: 348/2018;

FAPESC, Grant/Award Number:

Biodiversidade Marinha do Estado de Santa Catarina Project PI: A.L. FAPESC

4302/2010-8; FAPESC/CNPq, Grant/Award

Number: SISBIOTA-Mar project PI:

S.R.F. CNPq 563276/2010-0; FAPESC 6308/2011-8; Petrobras (BR), Grant/Award

Number: MAArE Project; King Abdullah

University of Science and Technology;

Coordenaç~ ao de Aperfeiçoamento de Pessoal

de Nível Superior

Abstract

H u m a n - m e d i a t e d s p e c i e s i n v a s i o n s a r e r e c o g n i z e d a s a l e a d i n g c a u s e o f g l o b a l

b i o t i c h o m o g e n i z a t i o n a n d e x t i n c t i o n . S t u d i e s o n c o l o n i z a t i o n e v e n t s s i n c e e a r l y

s t a g e s , e s t a b l i s h m e n t o f n e w p o p u l a t i o n s a n d r a n g e e x t e n s i o n a r e s c a r c e b e c a u s e

o f t h e i r r a r i t y , d i f f i c u l t d e t e c t i o n a n d m o n i t o r i n g . C h r o m i s l i m b a t a i s a r e e f -

a s s o c i a t e d a n d n o n - m i g r a t o r y m a r i n e f i s h f r o m t h e f a m i l y P o m a c e n t r i d a e f o u n d i n

d e p t h s r a n g i n g b e t w e e n 3 a n d 4 5 m . T h e o r i g i n a l d i s t r i b u t i o n o f t h e s p e c i e s

e n c o m p a s s e d e x c l u s i v e l y t h e e a s t e r n A t l a n t i c , i n c l u d i n g t h e A z o r e s , M a d e i r a a n d

t h e C a n a r y I s l a n d s . I t i s a l s o c o m m o n l y r e p o r t e d f r o m W e s t A f r i c a b e t w e e n S e n e -

g a l a n d P o i n t e N o i r e , C o n g o . I n 2 0 0 8 , v a g r a n t i n d i v i d u a l s o f C . l i m b a t a w e r e

r e c o r d e d o f f t h e e a s t c o a s t o f S a n t a C a t a r i n a I s l a n d , S o u t h B r a z i l ( 2 7 4 10 4 400 S ,

4 8 2 70 5 300 W ) . T h i s s t u d y e v a l u a t e d t h e i n c r e a s i n g d e n s i t i e s o f C . l i m b a t a

p o p u l a t i o n s i n S a n t a C a t a r i n a S t a t e s h o r e l i n e . T w o r e c e n t e x p a n s i o n s , n o r t h w a r d s

t o S~ a o P a u l o S t a t e a n d s o u t h w a r d s t o R i o G r a n d e d o S u l S t a t e , a r e d i s c u s s e d , a n d

a n i c h e m o d e l o f m a x i m u m e n t r o p y ( M a x E n t ) w a s p e r f o r m e d t o e v a l u a t e s u i t a b l e

C . l i m b a t a h a b i t a t s . B r a z i l i a n p o p u l a t i o n s a r e e s t a b l i s h e d a n d s i g n i f i c a n t l y i n c r e a s -

i n g i n m o s t s i t e s w h e r e t h e s p e c i e s h a s b e e n d e t e c t e d . T h e d i s t r i b u t i o n a l b o u n d -

a r i e s p r e d i c t e d b y t h e m o d e l a r e c l e a r l y w i d e r t h a n t h e i r k n o w n r a n g e o f

o c c u r r e n c e , e v i d e n c i n g e n v i r o n m e n t a l s u i t a b i l i t y i n b o t h h e m i s p h e r e s f r o m a r e a s

w h e r e t h e s p e c i e s s t i l l d o e s n o t o c c u r . E c o l o g i c a l p r o c e s s e s s u c h a s c o m p e t i t i o n ,

p r e d a t i o n a n d s p e c i a l l y h a b i t a t s e l e c t i v i t y m a y r e g u l a t e t h e i r p o p u l a t i o n s a n d

Received: 18 November 2019 Accepted: 29 April 2020

DOI: 10.1111/jfb.14365

FISH

362 © 2020 The Fisheries Society of the British Isles 2020;97:362 373.wileyonlinelibrary.com/journal/jfb J Fish Biol. –

Printed by [Universidade D

os Acores - 193.136.242.241 - /doi/epdf/10.1111/jfb.14365] at [24/09/2020].

o v e r a l l d i s t r i b u t i o n r a n g e . A l o n g - t e r m m o n i t o r i n g p r o g r a m m e a n d p o p u l a t i o n

g e n e t i c s s t u d i e s a r e n e c e s s a r y f o r a b e t t e r u n d e r s t a n d i ng o f t h i s i n v a s i o n a n d i t s

c o n s e q u e n c e s t o n a t u r a l c o m m u n i t i e s .

K E Y W O R D S

alien species, biological invasions, damselfishes, maximum entropy niche model, southwestern

Atlantic

1 | I N T R O D U C T I O N

H u m a n - m e d i a t e d c l i m a t e c h a n g e i s t h e m a i n c a u s e o f i r r e v e r s i b l e

c h a n g e s i n m a r i n e e c o s y s t e m s , s u c h a s o c e a n w a r m i n g a n d a c i d i -

f i c a t i o n , b i o d i v e r s i t y l o s s , d e c l i n e s a n d d i s t r i b u t i o n a l s h i f t s i n

m a r i n e s p e c i e s p o p u l a t i o n s ( B o o t h e t a l . , 2 0 1 7 ; P e c l e t a l . , 2 0 1 7 ) .

B i o l o g i c a l i n v a s i o n s m e d i a t e d b y a n t h r o p i c a c t i v i t i e s a r e r e c o g -

n i z e d a s a l e a d i n g c a u s e o f g l o b a l b i o t i c h o m o g e n i z a t i o n a n d

e x t i n c t i o n ( B a i l e y e t a l . , 2 0 1 1 ) . S u c h p h e n o m e n a , a l o n g s i d e f a c -

t o r s s u c h a s h a b i t a t l o s s a n d o v e r e x p l o i t a t i o n o f n a t u r a l

r e s o u r c e s , h a v e b e e n a c t i n g s y n e r g i c a l l y a s d r i v e r s o f w o r l d w i d e

b i o d i v e r s i t y l o s s ( B u t c h a r t e t a l . , 2 0 1 0 ) . T h e r e f o r e , m u c h a t t e n -

t i o n h a s b e e n p a i d t o a b e t t e r u n d e r s t a n d i n g o f p r o c e s s e s a n d

t h e m e c h a n i s m s i n v o l v e d i n e a c h s t a g e o f h u m a n - m e d i a t e d i n v a -

s i o n s ( i . e . , t r a n s p o r t , c o l o n i z a t i o n , e s t a b l i s h m e n t a n d c o n t r o l )

( A n d e r s o n e t a l . , 2 0 1 7 ; C a r l t o n , 1 9 9 6 ) .

In the Hawaiian Islands, from 1955 to 1961, 11 grouper, snapper

and emperor fish species were intentionally released by the Hawaii

Division of Fish and Game to enhance Hawaiian shallow-water game

and food fisheries (Johnston & Purkis, 2016). Within 15 years, three

of the introduced species established populations, whereas eight did

not. Two species, (Forsskål, 1775) andLutjanus kasmira Cephalopholis

argus Schneider, 1801, are now considered invasive (Johnston &

Purkis, 2016).

There are now over 1000 alien species inhabiting the Mediterra-

nean Sea, and most of them are thermophilic ( ., can have theiri.e

populations increased and established or have their distributional

range increased by global warming) that have entered the eastern

basin through the Suez Canal (Katsanevakis ., 2014; Kletou .,et al et al

2016). According to Kletou . (2016), Lessepsian invasions areet al

increasing rapidly, and . 130 species of marine fish are nowca

inhabiting the Mediterranean. For example, the blue spotted

cornetfish Rüppell, 1838, colonized nearly theFistularia commersonii

entire Mediterranean in just 7 years, threatening over 41 taxa of

native fish species (Kletou ., 2016). Another example is theet al

pufferfish (Gmelin, 1789) which preys uponLagocephalus sceleratus

Mediterranean commercially important cephalopod species and is

now classed as a fisheries pest (Kletou ., 2016). Despite all effortset al

to access, understand and control ecological invasion processes, stud-

ies about colonization events since early stages are scarce because of

their difficult detection and complex and expensive monitoring

(Anderson ., 2017).et al

The Azores chromis (Valenciennes, 1833) is aChromis limbata

marine reef-associated and non-migratory Pomacentrid fish,

i n h a b i t i n g r o c k y r e e f s a t d e p t h s r a ng in g fr om 3 t o 45 m ( All e n,

1 9 9 1 ; A n d e r s o n e t a l . , 2 0 1 7 ; B r i t o e t a l . , 2 0 0 2 ) . I t s o r i g i n a l d i s t r i b u -

t i o n e n c o m p a s s e s t h e e a s t e r n A t l a n t i c , i n c l u d i n g t h e A z o r e s ,

M a d e i r a a n d C a n a r y I s l a n d s , a n d W e s t A f r i c a b e t w e e n S e n e g a l a n d

P o i n t e N o i r e , C o n g o ( A l l e n , 1 9 9 1 ; A n d e r s o n e t a l . , 2 0 1 7 ; E d w a r d s ,

1 9 8 6 ) ( F i g u r e 1 ) . A d u l t s i n h a b i t r o c k y r e e f s a n d s a n d - w e e d b o t t o m s

( A l l e n , 1 9 9 1 ; A n d e r s o n e t a l . , 2 0 1 7 ) . T h e y a r e o v i p a r o u s a n d h a v e

d i s t i n c t p a i r i n g d u r i n g b r e e d i n g . A f t e r s p a w n i n g , t h e i r e g g s a d h e r e

t o t h e s u b s t r a t e w h e r e p a r e n t a l c a r e b y m a l e s i n c l u d e s v i g i l a n c e

a n d a e r a t i o n ( A n d e r s o n e t a l . , 2 0 1 7 ; B r e d e r & R o s e n , 1 9 6 6 ) . D u r i n g

s u m m e r , n e s t i n g m a l e s d e f e n d t e r r i t o r i e s a n d t a k e c a r e o f t h e

d e m e r s a l e g g s ( M a p s t o n e & W o o d , 1 9 7 5 ) . C h r o m i s c h r o m i s

( L i n n a e u s , 1 7 5 8 ) , t h e m o s t l i k e l y s i s t e r s p e c i e s o f C . l i m b a t a

( E d w a r d s , 1 9 8 6 ; W o o d , 1 9 7 7 ) , a f t e r a p e l a g i c l a r v a l p h a s e o f

1 8 –1 9 d a y s s e t t l e s o n a d u l t g r o u n d s ( A n d e r s o n e t a l . , 2 0 1 7 ; D o m i -

n g u e s e t a l . , 2 0 0 6 ; R a v e n t ó s & M a c p h e r s o n , 2 0 0 1 ) . I m m a t u r e s p e c i -

m e n s o f C . l i m b a t a a r e mor e un if or ml y br ow ni sh , wi th s il ve ry

s h i n i n g l o n g i t u d i n a l b a n d s . J u v e n i l e s a n d a d u l t s p r e y u p o n z o o -

p l a n k t o n ( A l l e n , 1 9 9 1 ; A n d e r s o n e t a l . , 2 0 1 7 ) . W i r t z ( 2 0 1 2 )

o b s e r v e d C . l i m b a t a f o r m i n g l a r g e p l a n k t o n - f e e d i n g a g g r e g a t i o n s o f

m o r e t h a n 1 0 0 i n d i v i d u a l s a n d m a l e s d e f e n d i n g r o c k y r e e f

s p a w n i n g a r e a s i n p l a c e s d e e p e r t h a n 1 0 m .

Brazilian reef fishes have been studied and monitored by local

marine scientists since the end of the past century (Floeter .,et al

2001; Moura ., 1999). In 2008, vagrant individuals ofet al C. limbata

were observed at Campeche Island, located 1.5 km on the east coast

of Santa Catarina Island, southern Brazil (27 410 4400 S, 48 270 5300 W)

(Leite ., 2009). Since then, Santa Catarina's populations ofet al

C. limbata have colonized most islands and islets in the vicinities of

Santa Catarina Island (Florianópolis), with densities significantly

increasing (Anderson ., 2017). Also, in 2008, vagrant individuals ofet al

C. limbata were reported in the vicinities of S~ ao Sebasti~ ao Island, S~ao

Paulo State, Brazil. After reports of recent new records from the S~ao

Sebasti~ ao Island, questions emerged among invasive species scien-

tists: (a) Have the populations reached a growth asymptote (carrying

capacity), or are they themselves fluctuating? (b) Are there more

niches available for along the Brazilian coast andC. limbata

elsewhere?

This study evaluated the increasing densities of C. limbata

populations in Santa Catarina State. A niche model of maximum

ANDERSON .ET AL 363FISH



entropy (MaxEnt) was developed to evaluate habitat suitability for

C. limbata along the southwest Atlantic coast (Verbruggen et al., 2009),

and recent new records of the species from S~ ao Paulo State were dis-

cussed. For a better understanding of such invasion effects on local reef

fish communities, a long-term monitoring programme is urgent.

2 | M A T E R I A L S A N D M E T H O D S

2.1 Study area|

This study was carried out on the coasts of three Brazilian states: Santa

Catarina (long-term monitoring), S~ ao Paulo and Rio Grande do Sul (new

records). The monitoring of the expansion of the established population

of C. limbata, f rom 2010 to 2019, was conducted in subtropic al reefs at

Florianópolis, Santa Catarina (27 350 41.0800 S, 48 320 38.9600 W). T he

geomorpholog y of th ese rocky reefs is char acterized, in its major p ortion,

by steep granitic rocky reefs ending in 12–15 m deep sandy bottoms.

The water visibility annua l averag e is 4 m. The temperature range is

between 1 0 C dur ing the harsh austral winters and 28 C in summer.

These rocky reefs are regar ded as the southernmost limit of distribu tion

of tr opical reef fish species that inhabit the tropical nort hern p ortion of

the Brazilian coast (Anderson et al., 2014, 2015, 2017, 2019). Fiv e islets

were selected for s ampling because of their logistic a ccessibility (e.g ., dis-

tance from the shore and confirmed C. limbata's established pop ulations)

(Anderson et al., 2017): Arv oredo, Deser ta, Galé, Aranhas and Xavier.

New records and range extension of to the state of SC. limbata ~ao

Paulo are now confirmed from Cabras Island, located in the vicinities

of S~ ao Sebasti~ ao Channel (23 490 5000 S, 45 230 3600 W). New

records and range expansion towards the southern Brazilian coast are

now confirmed for the state of Rio Grande do Sul (Parcel de Torres –

29 420 4.6000 S, 48 280 40.3200 W) (Figure 1).

2.2 Field data col lection techniques (Santa| Catarina State)

Underwater visual censuses (UVCs) [20 2 m (40 m×2 )] were used to

quantify fish density along Santa Catarina State. For this methodol-

ogy, a scuba diver swam 1 m above the substratum along 20 m,

recording fish 1 m to each side of the transect (Anderson ., 2017).et al

During the transects, the diver also sexed the fish according to their

colour patterns; females were yellow [ . 13 cm TL (total length)]ca

(Figure 5a c), and males were grey blue (young males) to a strong–

cobalt blue while defending the nest ( . 15 cm TL) (Figure 5d).Theca

present work is based on 9 years of UVCs conducted by the authors

and the database of the Marine Macroecology and Biogeography Lab-

oratory. In total, over 1000 UVCs from 2010 to 2019 were con-

ducted, and then a cut-off of 30 UVCs per site per year was selected

for analyses. Samples were collected in the shallow part of the reef

ranging from 5 to 14 m depth. All samples were obtained in the same

sites, in the mornings during the austral summers ( ., from earlye.g

December to March) (Anderson ., 2015, 2017, 2019).et al

2.3 New records|

Observations in S~ ao Paulo State occurred inside the Marine Protected

Area of Cabras Island Monitoring Programme, project ECOPERE-SE

(Reef Fish Ecology from Southwestern Brazilian Coast), implemented

F I G U R E 1 Map of Chromis

limbata's distribution in 2018. The monitoring of Brazilian established

populations in time was conducted in Santa Catarina State (7); monitoring of

range extensions (new records) was conducted in S~ ao Paulo State (8)

364 ANDERSON .ET AL

FISH



(a)

(b)

(c)

140Size (cm)

15 Adult

10

5

0

Recruits

Mean density ± SE

Total mean

Total density ± SD

450

400

350

300

250

200

150

100

140

120

100

80

60

40

20

0

50

0

To

tal d

en

sity

pe

r y

ear

± S

DD

en

sity

\siz

eTo

tal d

en

sity

pe

r y

ear

± S

D

*GLMPr(>|t|) < 0.05< AIC 161.16

Total mean

2010 2011 2012 2013 2014 2015

Timeline

2016 2017 2018 2019

Recruits total density ± SD

•GLMPr(>|t|) = 0.07< AIC 51.103

and young

120

100

80

60

40

20

0

F I G U R E 2 (a) Santa Catarina's

population variations from 2010 to 2019. Circles represent the number of individuals

detected. Different colours represent different sizes (ontogenetic stages) of

individuals. Asterisks indicate significance [generalized linear model (GLM)]. Chromis

limbata imagillustration by JPB DOP.

(b) Light green circles represent the total density of per year. The dashedC. limbata

red line represents the total 9 years mean’

density. Asterisks represent the GLM

significance Pr(>| |) < 0.05, and letterst

represent the Tukey contrasts test.post hoc

(c) Purple circles represent the total density per year of recruits (individual 5 cm TL).≤

The dashed red line represents the total

9 years mean density. Black dots represent’

the GLM significance Pr(>| |) = 0.07 (nott

significant)

MaxEnt

50°0N

50°0S

0°0

100°0W 50°0W 0°0 50°0E

00.25

0.5

0.751

F I G U R E 3 Maximum entropy niche model (MaxEnt). Representative

model map of maximum entropy for Chromis limbata. Warmer colours

indicate better predicted conditions




in January 2005. The Monitoring Programme comprised monthly sam-

pling periods, including diurnal and nocturnal scuba dives (depth

range: 4 13 m) and freediving (depth range: surface to 3 m), surround-–

ing Cabras Island, to record all rocky reef fish species. The dives' aver-

age time was 60 min for scuba and 40 min for freediving.

Photographs of were taken using a point-and-shoot cameraC. limbata

(Canon G9) in Ikelite housing and two Sea & Sea Strobes YS-110.

Photos were taken in macro mode as close to the fish as possible

and recorded in RAW and JPEG file modes. In every photographic

record, the diver took notes of the fish size. As a measure of reference

and to avoid distortions in the assessment, the diver positioned a 5 cm

ruler o n the substrate close to the site occupied by the fish. Images were

analysed after edition using free software Image J 1.49 ( http://imagej.

nih.gov/ij/) to obtain meristic data and measurements to confirm the fish

identification followed (Canestrini, 1872; Froese & Pauly, 2019).

In December 2016 one vagrant individual of C. lim bata was detected

and photographed in Queimada Grande Island, also in S~ ao Paulo State

(24 290 14.5500 S, 46 400 36.7600 W), by L. Francine. New records f rom

Rio Grande do Sul State were collected from recreational divers' videos

posted online. Those were recorded on 4 March 2017 at the Parcel de

Torres – a rocky outcrop located 20–25 km offsh ore (29 420 4.6000 S,

48 280 40.3200 W), at depths ranging from 22 to 30 m (video https://

www.youtube.com/watch?v=uZoNhCf_iNE&t=386s).

2.4 Data analyses|

2.4.1 Population expansion in Santa Catarina|

Generalized linear models (GLM) were used to evaluate the effect of

time on C. l imbata's densities in Santa Catarina State. Individuals’

densities were used as a dependent variable and time (year) as an inde-

pendent variable according to Chatfield (1989) and Rencher and

Schaalje (2008). For significant differences, Tukey contrasts were used to

analyse variations between years. Tukey test contrasts werepost hoc

performed using the “multicomp” R p ack ag es (H oth orn et al., 2016),

“ ” “ ”lsmeans (Lenth & Lenth, 2018) and multicompView (Graves et al.,

2015). Assumptions of normality and homoscedasticity were assessed

using K olmogorov–Smirnov/Lilliefors and Bartlett's tests. Data were log

transformed (log X + 1) to mee t the assumptions of norm ality

(Snedecor & Cochran, 1989; Underwood, 1981; Zar, 1999). The analysis

was performed in R environment (R Core Team 2019).

2.4.2 Nich e modelling procedures|

Macroecological niches of were modelled using the MaxEntC. limbata – a

machine learning algorithm (R package dismo v1.1–4) which consists of a

technique based on the principle of maximum entropy – using species'

presence data as proposed by Philips and Dudík (2008). This algorithm has

been tested worldwide in several studies and is considered an adequate

tool to be used in such contexts (see Elith & Leathwick, 2009; Hernandez

et al., 2006; Philips & Dudík, 2008). Only accurate data (i.e., published

papers) collected in literature regarding occurrence of species were applied

to elaborate the model (Verbruggen et al., 2009) (Appendices 1 and 2).

2.4.3 Presence data and environmental variables|

A total of 708 georeferen ced occurrences were used to model C. limbata

niche availability. Occurrence records were obtained from scientific journal

articles (Appendix 2). For later use in the modelling procedures, the

MaxEnt

00.250.50.751

MaxEnt

00.250.50.751

MaxEnt

00.250.50.751

6°0S

21°0S

55°0N

40°0N

56°0N

41°0N

36°0S

52°0W

(a) (b) (c)37°0W 76°0W 61°0W 11°0W 4°0E

F I G U R E 4 Maximum Entropy Niche model (MaxEnt): a) suitable habitats for the Brazilian coast; b) suitable habitats fortheC. Limbata

Northwestern Atlantic coast; c) suitable habitats for the Northeastern Atlantic coast

366 ANDERSON .ET AL

FISH



background (i.e., “pseudo-occurrences”) was generated with respect to a cir-

cumference of 500 km around the occurrence records as proposed by Elith

et al. (2011). To avoid spatial autocorrelation, occurrences located <1 km

apart were randomly selected and removed, as well as duplicate entries.

The data set of environmental variables (global scale) (see Appen-

dix 3) was used to generate the model and was downloaded from Bio-

Oracle data set (Assis ., 2018; Tyberghein ., 2012). Predictiveet al et al

variables were selected considering relationships among 'sC. limbata

biology, ecology and collinearity between environmental variables

(Assis ., 2018; Tyberghein ., 2012).et al et al

The best-fit model was selected according to the following steps.

(a) The multicollinearity test was conducted using Pearson's correla-

tion coefficient ( ) to examine the cross-correlation between environ-R

mental variables (Farashi & Naderi, 2017). (b) Variables with a cross-

correlation coefficient value >0.9 were excluded from further analysis

(see Appendix 3) (Farashi & Naderi, 2017). (c) GLMs were used to test

the significance of environmental variables (Appendix 4) and then to

select the best-fitted model according to the AIC ( ., the preferredi.e

model is the one with a minimum AIC value) (Appendix 4) (Akaike,

1998). (d) Such procedures resulted in a subset of 15 variables used as

the best-fitted input for the model (Figure 4, Appendices 4 and 6).

Both presence data and environmental variables were processed and

analysed in R (R Development Core Team, 2019). (e) The performance

of the models was measured using the area under the curve (AUC)

(Philips & Dudík, 2008; Phillips ., 2011; Verbruggen ., 2009).et al et al

3 | R E S U L T S

3.1 The invasive populations in Santa Catarina|

A t o t a l o f 7 8 0 s t r i p t r a n s e c t s w e r e c o n d u c t e d d u r i n g t h e a u s t r a l

summ ers (i.e. , D e c e m b e r t o A p r i l ) f r o m 2 0 1 0 t o 2 0 1 9 , c o v e r i n g a

t o t a l a r e a o f 3 1 , 2 0 0 m2 a n d c o r r e s p o n d i n g t o c a . 1 1 7 h o f u n d e r w a -

ter obser vat i on. Thi s wor k r esult ed i n 1 0 ye ars’ m o n i t o r i n g o f

C. lim bat a's p opul ation s in the coas t of S anta Cat arin a, so uthe rn Br a -

zil (F igur e 2 ).

The invasive Pomacentrid populations in Santa Catarina vary sig-

nificantly in time [GLM Pr(>| |) < 0.05] (Figure 2b; Appendix 5). Con-t

sidering species' population structure in time, large schools of small

individuals ( ., 5 cm) were detected in 2016, 2017, 2018 and 2019.e.g ≤

Despite the large numbers of recruits detected, no significant differ-

ences were found over time [GLM Pr(>| |) = 0.07] (Figure 2c; Appen-t

dix 5). The number of adult female and young male feeding

aggregations has increased since 2010 (Figure 2a). Large adult males'

densities also increased along Santa Catarina coast in the same period

(Figure 2a). Despite their populational significant variations in time

(Figure 2b), no significant differences were detected among years

(Figure 2b; Appendix 5).

3.2 Fundamental niche availability model|

T h e m o d e l p r e d i c t s h i g h l y p r o b a b l e s u i t a b l e h a b i t a t s f o r C . l i m b a t a

i n t h e n o r t h w e s t e r n A t l a n t i c t o t h e c o a s t s o f N e w J e r s e y , C o n n e c t -

i c u t a n d M a s s a c h u s e t t s ( F i g u r e s 3 a n d 4 ) , t h e s o u t h e r n B r a z i l i a n

c o a s t , f r o m E s p í r i t o S a n t o S t a t e t o R i o G r a n d e d o s S u l S t a t e a n d i n

t h e n o r t h e a s t e r n A t l a n t i c t o t h e c o a s t o f F r a n c e ( F i g u r e s 3 a n d 4 ) .

A m o n g t h e 1 5 e n v i r o n m e n t a l p r e d i c t o r s a n a l y s e d , t h e m o s t s i g n i f i -

c a n t v a r i a b l e s a r e r e l a t e d t o p r i m a r y p r o d u c t i v i t y a n d o c e a n o -

g r a p h i c c o n d i t i o n s ( T a b l e 1 ; A p p e n d i x 6 ) . T h e m o d e l s p r e s e n t e d a

g oo d p er f or m an c e wi t h an A U C va l ue o f 0 .9 9 . Re s ul t s we r e cl o se r

t o a p e r f e c t p r e d i c t i o n , i n d i c a t i n g t h a t m o s t e s s e n t i a l e n v i r o n m e n -

t a l v a r i a b l e s w h i c h d e t e r m i n e s p e c i e s d i s t r i b u t i o n s w e r e c o n s i d -

e r e d i n t h e d a t a s e t ( T a b l e 1 ; A p p e n d i x 6 ) ( V e r b r u g g e n

e t a l . , 2 0 0 9 ) .

T A B L E 1 Environmental variables used in the MaxEnt model and their

contribution to the model predictions.

Environmental variables Unit Contribution (%) Permutation importance

Diffuse attenuation mean m−1 23.3 47.9

Dissolved oxygen mean mol m−3 22.2 0

Current velocity maximum m−1 13 12.4

Primary productivity maximum g m−3 day−1 10.3 10.4

Current velocity minimum m−1 8.2 9.4

Par maximum E m−2 day−1 8.2 5.7

Cloud cover maximum % 4.3 5.8

Par mean E m−2 day−1 1.9 1.2

Temperature maximum C 1.8 0.9

Calcite mean mol m−3 1.7 0.8

Phosphate maximum mol m−3 1.5 0

Chlorophyll mean mol m−3 1.2 1

Phosphate minimum mol m−3 0.8 2.2

Silicate minimum mol m−3 0.8 0.2

Surface pH 0.8 2.1–

Bold values are shown Variables with higher permuta tion importance.




3.3 Brazilian populations' range expansion (new|records)

Vagrant individuals of were recorded in the southeasternC. limbata

Brazilian coast from 2008 to 2019. During the Monitoring Programme

of the Marine Protected Area of Cabras Island, four individuals of

C. limbata were recorded. The site for all records was S~ ao Sebasti~ao

Channel, east coast of S~ ao Sebasti~ ao Island (23 490 5000 S,

45 230 36 00 W). Among these records, a vagrant individual of

C. limbata [8 10 cm standard length (SL)] was repeatedly detected at–

the vicinity of Cabras Island every month from June 2008 to June

2009. In the same area, another fish, 12 cm, was recorded in January

and April 2011. From March to May 2012, another individual, 10 cm,

was recorded, and finally in May 2014 an 8 cm fish was monitored

until July 2015, when it reached 10 cm (Figure 5). Since then, no fur-

ther records have been reported from Cabras Island.

All enc ount e rs occ urre d in the same rocky -b ott o m area of .c a

2 0 m 2 . I n d i v i d u a l s w e r e u s u a l l y o b s e r v e d f e e d i n g t o g e t h e r w i t h l a r g e

a g g r e ga t i o n s o f Abud efd uf saxat il is ( L i n n a e u s , 1 7 5 8 ) , a n d o n l y i n t h e

l a s t r e c o r d s C . l i m b a t a was detec ted fee ding toge the r wi th a single

i n d i v i d u a l o f i t s c o n g e n e r Ch romi s mult ili neata ( G u i c h e n o t , 1 8 5 3 ) .

T h e d i f f e r e n c e s b e t w e e n t h e s i z e s a n d t i m e o f o c c u r r e n c e i n d i c a t e d

t h e p r e s e n c e o f m o r e t h a n o n e i n d i v i d u a l d u r i n g t h e t i m e o f

obse rvat ions .

In December 2016 one adult male was photographed in Que-

imada Grande Island, S~ ao Paulo State coast, representing a new

record and range extension of 's populations for the Brazil-C. limbata

ian coast (Figure 5d). In February, 2017 a video was uploaded showing

several individuals of in the Parcel de Torres, Rio Grande doC. limbata

Sul State (29 34.501 0 S, 048 07.5670 W), extending the southern-

most distribution limit of the invasive Pomacentridae and

corroborating the model predictions regarding the fundamental niche

availability for southern Brazil (https://www.youtube.com/watch?v=

uZoNhCf_iNE). The video shows mature females, large males (blue

individuals) and a small school of recruits, which suggests a growing

population.

4 | D I S C U S S I O N

4.1 Santa Catarina's established popul ations and| the Arc of Capricorn region influence“ ”

New populations of invasive marine fish species along the western

Atlantic coast have been monitored with greater concern since the

establishment of the Indo-Pacific lionfish species, Pterois volitans

(Linnaeus, 1758) and (Bennett, 1828), along the AtlanticPterois miles

coast of the United States (Schofield, 2009). From 1999 to 2015 the

species also colonized the Caribbean, extending their range to the

southern Brazilian coast (Ferreira ., 2015; Schofield, 2009). Experi-et al

ments with intentional introductions of 11 marine predatory fish ( .,e.g

grouper, snapper and emperor fish) were conducted in the Hawaiian

Islands from 1955 to 1961 to produce new fishery resources

(Johnston & Purkis, 2016). Within 15 years eight species' populations

crashed, and three established self-sustained populations. Two spe-

cies, (Forsskål, 1775) the common bluestripe snapper andL. kasmira

C. argus (Schneider, 1801) the Peacock hind, are classified as invasive

(Johnston & Purkis, 2016). In 2013 the Indo-West Pacific damselfish,

known as Regal demoiselle (Bleeker, 1856),Neopomacentrus cyanomos

was first recorded in the west Atlantic, when it was reported to be

common on reefs near Coatzacoalcos, in the extreme southwest Gulf

of Mexico corner (Robertson ., 2016). From 2013 to 2015 theet al

F I G U R E 5 Pictures of Chromis

limbata ( ) from (a) Santa Catarina♀

State (image A. B. Anderson), (b and c)

S~ ao Sebasti~ ao (Cabras Island) ( ), S♀ ~ao Paulo State (images J. P. Silva) and

(d) Queimada Grande Island ( ), S♂ ~ao Paulo State (image L. Francini)

368 ANDERSON .ET AL

FISH



species was observed on six nearshore reefs adjacent to Veracruz City,

Veracruz, Mexico (Robertson et al., 2016). Robertson et al. (2016) also

suggested that N. cyanomos may compete with native planktivorous

damselfishes [e.g., the Brown chromis C. multilineata (Guichenot, 1853)]

and have adverse effects on populations. This 10-year monitoring study

of C. limbata's populations in the southern Brazilian coast, compared to

the works mentioned earlier, seems to follow the same invasive pattern

of esta blishme nt and expansio n. In a near f uture, C. limbata may repre-

sent a threat to l ocal native damselfishes competing for resources such

as food, shelter and nesting areas (Anderson et al., 2017).

The establishment of a new population will depend on abiotic (e.g.,

topography, temperature, nutrient availability) and biotic [e.g., initial colo-

nizers (healthy propagules, larvae, adults), mating success, new mutations,

elimination of deleterious alleles, repeated inflow of new genotypes, compe-

tition, predation] factors (Anderson et al., 2017; Kaňuch et al., 2014). The

low genetic diversity detected in Santa Catarina's established populations

compared to native populations from Macaronesia (Anderson et al., 2017)

suggests a small larval pulse or the arrival of a small group of individuals.

Populations in Santa Catarina seem to be varying significantly

(Figure 2). Blue males with large harems of females and large schools of

small individuals (<5 cm) were detected in all s tudied sites from 2013 to

2019 (Figure 2a). This may well point to a healthy increasing population,

with pote ntial f or spatial domination (e.g., higher density and biomass

than local congener C. multilineata and other Pomacentrids such as

A. saxatilis et al) in the near future (Anderson ., 2017).

The southwestern Atlantic biogeographic ecotone is also known as

the Arc of Capricorn ( ., encompassing the states of Rio de Janeiro, Si.e ~ao

Paulo, Paraná , Santa Cata rina and Rio Grande do Sul) and represents the

southernmost limit of dist ribution for most tropical organisms ( Anderson

et al., 2015, 2017). Moreove r, the region is considered a warm temper ate

biogeographic province (Bernardes et al., 2018; Horta et al., 2001 ). This

part of the Brazilian coast, especially Santa Catarina State, presents sea-

sonal patterns of temperate variations with a monthly average of

25.6 ± 0.5 C in winter and 27.0 ± 0.9 C in summer (Anderson et al.,

2015, 2017; Ber nardes et al., 2018). Thi s seasonal pattern is determined

by both warm tropical waters from the Brazilian Current (originating from

the north and flowing southwards) and cool waters from the South Atlan-

tic Central Water, flowing n orth. This mass of water intrudes on the shal-

low c oastal shelf of this region, espec ially during the spring and summer

northeastern winds, and features temperatures of ≤16 C (Anderson et al.,

2015; Bernardes et al., 2018). Such characteristics seem to work as an

optimum habitat for C. limbata and may have i nfluenced th e establishment

of a healthy popula tion. Other wise, furth er north along the coast of S~ao

Paulo State , with slightly warmer water masses, C. limbata was also

detected, albeit in mod est numbers (Anderson et al., 2017 ).

4.2 Fundamental niche availability|

The main predictors which have influenced the model were variables

related to primary productivity, temperature, oceanographic and topo-

graphic conditions (Table 1). Therefore, the model reinforces the affin-

ity of the species to areas with cooler waters and high primary

production ( ., regions with upwelling) (Anderson ., 2017). Alle.g et al

main regions highlighted by the model have distinct oceanographic

characteristics regarding temperature, currents, upwellings and resur-

gence phenomena, which directly affect primary productivity [ ., thee.g

Golf Stream in the northwestern Atlantic, the Iberian Poleward Cur-

rent system in the northeastern Atlantic and the Brazil current in the

southwestern Atlantic (Bernardes ., 2018; Bukata ., 2018;et al et al

Peliz ., 2005)].et al

Many northwestern and northeastern Atlantic sites do not pre-

sent topographic conditions such as complex rocky coastlines with

small archipelagos, islands or nearshore islets. Moreover, temperature

seems to be a limiting factor for 's dispersal. These abioticC. limbata

and biotic factors such as predations and competition may explain– –

why does not occur, so far, in those regions.C. limbata

Consi deri ng t hat t he Br az ili an pop ula tion s of C . l i m b a t a ( S~ao

Paulo an d Santa Cat arin a S tat e s) have th e sam e age (i.e . , i n b o t h

c a s e s , f i r s t r e c o r d s w e r e d o c u m e n t e d i n 2 0 0 8 –2 0 0 9 ) , t h e l o w d e n s i -

ties from S~ ao Pau lo (warmer oce an ic water masses) may empha size

that th e large r Braz ili an popu lati ons ha ve affi niti es to col der ,

n u t r i e n t - r i c h a n d m o r e p r o d u c t i v e w a t e r s , s u c h a s t h o s e i n S a n t a

C a t a r i n a ' s c o a s t s , w h e r e u p w e l l i n g i s a c o n s t a n t p h e n o m e n o n a n d

prim ary p rodu ctiv ity i s hi gher when co mpar ed t o no rthe rner par ts o f

the Braz ilia n coast ( A nder son et al . , 2 0 1 7 ; B e r n a r d e s et al. , 2 0 1 8 ) .

Tempe ratu re may be a limit ing fac tor to the exp ansi on of C. limb at a

towar ds the northe rn Brazi l ian coas t, consi deri ng the a verag e sea

surf ac e temp erat ure of such reg ions (An ders on et al. , 2 0 1 7 ; M a t a n o

et al. , 2 0 1 0 ; O l s o n e t a l . , 1 9 8 8 ) . O t h e r w i s e , d e e p e r a n d c o l d e r r e e f s

(a de pth of 5 0 m maxi mum) may re prese nt a ref uge and also wor k as

“ ”s t e p p i n g s t o n e s f o r C . l i m b a t a ' s n o r t h w a r d e x p a n s i o n ( e. g. , V i t ó r i a -

Trind ade Sea Moun t Ch ain ) ( Pinhe iro et al. , 2 0 1 7 ) . M e d i t e r r a n e a n

a n d A f r i c a n p o p u l a t i o n s o f C h romi s spe cies hav e bee n rec orded fr om

1 0 t o 4 0 m d e p t h ( B e r t o n c i n i e t a l . , 2 0 1 0 ; D o m i n g u e s . , 2 0 0 5 ;et al

Domin gues e t a l . , 2 0 0 7 ) .

4.3 S| ~ ao Paulo vagrant specimens and new record

origins

Leite . (2009) described that all the encounters of inet al C. limbata

Santa Catarina State occurred in the same rocky-bottom area of .ca

20 m2 , suggesting a restricted occupation area based on specific sub-

strate conditions and/or behavioural interactions ( ., reproductivee.g

and feeding behaviours), which indicates site fidelity and small resi-

dential range. This study suggests that may have similar ter-C. limbata

ritorial behaviours on Brazilian-colonized areas. The differences

between sizes and time of occurrence of indicate the pres-C. limbata

ence of more than one individual during the observations. In this par-

ticular case, different sizes and record timing could be explained

through recurrent introductions of in the SC. limbata ~ ao Sebasti~ao

canal. It is possible to apply Williamson & Fritter's rule of ten (1996)“ ”

for this. In other words, the probability of success of an introduction

is very low, and most introductions fail to establish and spread. It has

been suggested that only 1 out of every 10 introductions survives,




only one-tenth of these become established and spread and only a

tenth of these become invasive (Williamson & Fitter, 1996).

Since 2008 has been recorded in the vicinities of SC. limbata ~ao

Sebasti~ ao, S~ ao Paulo State, Brazil; the most recent one was from Que-

imada Grande Island, in December 2016. According to Leite

et al C. limbata. (2009), the first record of in Santa Catarina occurred

in that same year, which suggests that both records may have the

same origin. Otherwise, recent records in S~ ao Paulo may well be a nat-

ural dispersal from Santa Catarina's established populations. The

genetic study published by Anderson . (2017) concluded thatet al

Santa Catarina's populations do not share haplotypes with

Macaronesian populations, which may imply that the source of both

populations probably originated from western Africa. When consider-

ing species' morphology (Figure 5), specimens from S~ ao Paulo and

Santa Catarina are remarkably similar. Nevertheless, no C. limbata

have been found yet along the relatively small Paraná coastline. This

is important for discussion because this state borders S~ ao Paulo

(north) and Santa Catarina (south).

4.4 The long-distance dispersal|

Ocean currents can drift fish larvae to new destinations although dis-

tance is a prime factor in determining which species will prevail. Dis-

tance apparently acts as a natural filter and probably excludes species

with short larval stages, such as damselfishes (Pomacentridae), and

selects others with long larval lives such as surgeon fishes

(Acanthuridae) (Luiz ., 2004, 2012, 2015). Cowen . (2006)et al et al

showed that typical larval dispersal distances for the wider Caribbean,

providing ecologically significant numbers of settlers, were only on a

scale of 50 100 km for most species with a relatively high rate of–

local retention or recruitment from adjacent locations. Recent inva-

sion events to the Brazilian coast were related to a supposed flow of

the superficial currents on the tropical Atlantic flowing westward from

Africa to Brazil or natural larval dispersal from the Caribbeanvia

towards the Brazilian coast (Anderson ., 2015; Anderson .,et al et al

2017; Ferreira ., 2015; Leite ., 2009; Luiz ., 2004).et al et al et al

Semi-submersible oil rigs are notorious to transport entire communi-

ties of marine organisms through oceans (Anderson et al., 2017; Wanless

et al., 2010). Recently, the presence of the Pomacentrids Abudefduf

hoefleri (Steindachner, 1881) and A. saxatilis in the Canaries has been

attributed to oil rigs (Pajuelo et al., 2016). Damselfishes, especially within

the genus Abudefduf, Neopomacentrus and Chromis, have been detected

rafting in plastic debris, algae and flotsam (Luiz et al., 2015; Robertson

et al., 2016), which led us to consider the “hitchhiker's hypothesis” as the

most plausible (Anderson et al ., 2017). Other records of invasive species

can be interpreted in a different way, suggesting ballast water among the

most important vectors of introduced species i n the marine realm, with a

high risk to coastal habitats (Ferreira et al., 2004a, 2004b, 2009, 2015;

Lopes et al., 2009).

B e c a u s e i n v a s i o n m e d i a t e d b y s h i p s i s t h e m a i n p a t h w a y o f

exot ic s peci e s, i t is evide nt t h at t here is a need t o mon itor areas

a d j a c e n t t o h a r b o u r s t o g e t h e r w i t h t h e a p p l i c a t i o n o f r i g o r o u s

cont rols of ba llas t water . Des pit e the incr easi ng rate in exo tic sp e-

cies r epor ts, Br azil does not h ave an effec tive con trol sy ste m for b al-

last water . NORM AM (Br azi lian Navy Au tho rity R ules/ Dir ecti ves)

d e t e r m i n e s t h a t s h i p s e x c h a n g e b a l l a s t w a t e r w i t h i n a n i s o b a t h o f

200 m, to re duce the risk of spread ing exoti c sp ecie s. Nonet h eless ,

the co ntro l of an y spe cies presen t is not ef f ecti ve ( de Pau la Co s ta

et al. , 2 0 1 1 ) .

Considering the growth in the number of ship visits to Brazilian

harbours (Wilmsmeier & Monios, 2016), the increase in their transit

speeds and the possibility of ballast water to function as an incubator

during the cruise for some planktonic species and the fact that

C. limbata et allarvae and juveniles prey upon zooplankton (Bax .,

2003; Gollasch ., 2000), it is plausible to consider the hypothesiset al

of shipping transport for larvae to Brazil (Anderson .,C. limbata et al

2017). In contrast, there are no evidences of any Pomacentridae listed

in samples collected directly from ship ballast waters (Williams .,et al

1988; Wonham et al ., 2000).

4.5 The impacts in local communities|

Considering the high level of primary productivity which occurred in

the recently colonized areas, the invader may not pose aC. limbata

threat to local planktivorous fish, regarding competitive behaviours

towards food resource (Anderson ., 2017). On the contrary, theet al

aggressive behaviour of adult males during reproduction may pose a

severe threat to their congeners, other Pomacentridae and species

which have the same demersal reproductive behavioural patterns [e.

g C. multilineata Stegastes fuscus A. saxatilis Stegastes., , (Cuvier, 1830), ,

pictus Stegastes variabilis(Castelnau, 1855), (Castelnau, 1855)]

(Anderson ., 2017; Laglbauer ., 2017). Moreover, the aggres-et al et al

sive reproductive behaviour of adult males may cause detri-C. limbata

mental effects on shelter availability for local fish. In rocky reef

systems, shelter availability ( ., holes and crevices) is a valuablee.g

resource to species which rely on the environment as protection

against predation and parental care (Anderson ., 2017, 2019). Theet al

need for behavioural studies in the invaded areas is urgent for a better

understanding of patterns, such as reproductive seasonality, spawning

characteristics and habitat use.

According to Pinnegar (2018), large populations of playC. chromis

a fundamental role in the Mediterranean Sea by transferring nutrients

from pelagic systems to the littoral in the form of solid and liquid

wastes. In addition, represents a major prey item for preda-C. chromis

tors and mesoconsumers in Mediterranean food webs (Pinnegar,

2018). It is also considered a major consumer of fish eggs and there-

fore may have a strong influence on the dynamics of other fish spe-

cies (Pinnegar, 2018). Therefore, the increasing numbers of the

invasive in southern Brazil may have, in a near future, theC. limbata

same effects of the system described by Pinnegar (2018), regarding

the populations of its Atlanto-Mediterranean congener .C. chromis

Long-term monitoring of such impacts is crucial for a better under-

standing of ecological impacts of invasive species in marine

ecosystems.

370 ANDERSON .ET AL

FISH



5 | C O N C L U S I O N S

This study indicated that populations in Santa CatarinaC. limbata

State vary over time and are expanding in space, obeying the general

patterns of invasive species. Specimens detected in S~ ao Paulo State in

the early stages of the colonization (2008) may have the same origin

as Santa Catarina's populations, and may also have originated the

most recent records (2017). Despite the wide availability of funda-

mental niches for worldwide, temperature seems to be aC. limbata

limiting factor for their dispersal. From all the dispersal hypotheses

which could account for this invasion in south Brazil, the oil rig trans-

portation and hitchhikers or rafting seem more plausible.“ ”

The present population of this invader in Brazilian waters and

their eventual effects on native reef fish communities are still not pos-

sible to evaluate. The rocky reefs of southern Brazil are positioned in

a biogeographic climatic transition zone, affected by several oceano-

graphic and climatic phenomena ( ., upwellings, current shifts, Lae.g

Niña and El Niño southern oscillations, cold ocean water intrusions

during the austral winters). Such climatic complexity affects local ich-

thyofauna population s density and biomass, which can underestimate’

the real effects of 's invasion on local communities. A long-C. limbata

term monitoring programme (including genetic studies) of this inva-

sion would be crucial to elucidate the drivers of such unique dispersal

and evaluate the impacts of a species invasion in a newin situ

environment.

A C K N O W L E D G E M E N T S

We thank FAPES (Fundaç~ ao de Amparo à Pesquisa e Inovaç~ ao do

Espírito Santo, Brazil)/CAPES (Coordenaç~ ao de Aperfeiçoamento de

Pessoal de Nível Superior, Brazil) (PROFIX programme number

10/2018 T.O.: 348/2018) for A.B.A. postdoctoral scholarship. We–

also thank the anonymous reviewers and A.R.W. (Red Sea Research

Center King Abdullah University of Science and Technology), who–

contributed to the improvement of this paper. Thanks to the Marine

Macroecology and Biogeography Laboratory (LBMM) staff for field

support. Funding sources: SISBIOTA-Mar (PI: S.R.F., CNPq

563276/2010-0; FAPESC 6308/2011-8), Ilhas do Sul Project (PI:

S.R.F., CNPq 475367/2006-5), MAArE Project Monitoramento–

Ambiental do Arvoredo e Entorno (PI: B. Segal), CAPES scholarship to

A.B.A., Biodiversidade Marinha do Estado de Santa Catarina Project

(PI: A.L., FAPESC 4302/2010-8) and ECOPERE-SE Project (Ecologia

de Peixes Recifais da Costa Sudeste do Brasil) (PI: J.P. Silva).

A U T H O R C O N T R I B U T I O N S

A.B.A. contributed the original idea and helped with data generation,

data analysis, manuscript preparation and reviews; S.R.F., J.P.S. and

J.P.S.B. contributed the original idea and helped with manuscript prep-

aration, reviews and funding; R.S. and C.L.B.F. contributed to manu-

script preparation.

C O N F L I C T S O F I N T E R E S T

All authors declare that they have no conflict of interest.

E T H I C A L A P P R O V A L

All applicable international, national and/or institutional guidelines for

the care and use of animals were followed.

S A M P L I N G A N D F I E L D S T U D I E S

All necessary permits for sampling and observational field studies

were obtained by the authors from competent authorities.

O R C I D

Antônio B. Anderson https://orcid.org/0000-0003-2502-7018

Jodir Pereira da Silva https://orcid.org/0000-0001-7510-7935

Sergio R. Floeter https://orcid.org/0000-0002-3201-6504

Jo~ ao P. Barreiros https://orcid.org/0000-0003-4531-6685

R E F E R E N C E S

Akaike, H. (199 8). Factor analysis and AIC. In E. Parzen, K. Tanabe, &

G. Kitagaw a (Eds.), (pp. 371 386).Selected papers of Hirotugu Akaike –

New York, NY: Springer.

Allen, G. (1991). . Hong Kong: Mergus Press.Damself ishes of the world

Anderson, A., Bonaldo, R., Barneche, D., Hackradt, C., Félix-Hackradt, F., García-Chartón, J., & Floeter, S. (2014). Recovery of grouper assem-

blages indicates effectiveness of a marine protected area in southern

Brazil. , , 207 215.Marine Ecology Progress Series 514 –

Anderson, A. B., Batista, M. B., Gibran, F. Z., Félix-Hackradt, F. C.,

Hackradt, C. W., García-Charto n, J. A., & Floeter, S. R. (2019). Habitat

use of five key species of reef fish in rocky reef systems of southern Brazil: evidences of MPA effectiveness. , (2),Marine Biodiversity 49

1027 1036.–

Anderson, A. B., Ca rvalho-Filho, A., Mor ais, R. A., Nunes, L. T., Quimbayo, J. P., & Floeter, S. R. (2015). Brazilian tropical fishes in their

southern limit of distribution: checklist of Santa Catarina's rocky reef

ichthyofauna, remarks and new records. , n. 4, p. 1688.Checklist 11

Anderson, A. B., Salas, E. M., Rocha, L. A., & Floeter, S. R. (2017). The

recent coloni zation of South Brazil by the Azores Chromis Chro mis

limbata Journal of Fish Biology 91. , , 558 573.–

Assis, J., Tyberghein, L., Bosch, S., Ver bruggen, H., Serr~ ao, E. A., & De

Clerck, O. (2018). Bio-ORACLE v2.0: extending marine data layers for

bioclimatic modelling. , , 277 284.Global Ecology and Biogeography 27 –

Bailey, S. A., Deneau, M. G., Jean, L., Wiley, C. J., Leung, B., &

MacIsaac, H. J. (2011). Evaluating efficacy of an environm ental policy

to prevent biological invasions. ,Environmental Science & Technology

45, 2554 2561.–

Bax, N., Williamson, A., Aguero, M., Gonzalez, E., & Geeves, W. (2003).

Marine invasive alien species: a threat to global biodiversity. Marine

Policy 27, , 313 323.–

Bernardes, M. B., Anderson, A. B., Franzan Sanches, P., Simionatto Polito, P.,

Lima Silve ira, T., Velez-Rubio, G., … Martinez, A. (2018). Kelps' long- distance dispersal: role of ecological/ocea nographic processes and impli-

cations to marine fore st conserva tion. Diversity, 10, 11.

Bertoncini,

A. A., Machado, L. F., Barreiros, J. P., Hostim-Silva, M., & Verani, J. R. (2010). Rocky reef fish community structure in two Azo r-

ean islands (Portugal) Central North Atlantic. Journal of the Marine Bio-

logical Association of the United Kingdom 90, , 1353 1362.–

Booth, D. J., Poloczanska, E., Donelson, J. M., Molinos, J. G., &

Burrows, M. (2017). Biodiversi ty and climate change in the oceans. In

B. F. Phillips & M. Pérez-Ramírez (Eds.), Climate change impacts on fish-

eries and aquaculture: A global analysis (Vol. 1, pp. 63 –89). Hoboken,

NJ: John Wiley & Sons Ltd.

Breder, C. M., & Rosen, D. E. (1966). Modes of reproduction in fishes

(p. 941). Neptune City, NJ: T. F. H. Publications , Inc..




Brito, A., Pascual, P. J., Falcón, J., Sancho , A., & González, G. (2002). Peces

de las islas Canarias. La Laguna, Spain: Catálogo comen tado e ilustrado,

Francisco Lemus Editor.

Bukata, R. P., Jerome, J. H., Kondratyev, A. S., & Pozdnyakov, D. V. (2018). Optical properties and remote sensing of inland and coastal waters, Boca

Raton, Florida: CRC Press.

Butchart, S. H. M., Walpole, M., Collen, B., van Strien, A., Scharlemann, J. P. W., Almond, R. E. A., Watso n, R. (2010). Global…

biodiversity: indicators of recent declines. , , 1164 1168.Science 328 –

Canestrini, G. (1872). . Milano, Italy: Vallardi.Fauna d'Italia; parte terza Pesci

Carlton, J. T. (1996). Biological invasions and cryptogenic species. ,Ecology

77, 1653 1655.–

Chatfield, C. (1989). Non-linear and non-stationary time series analysis: M.B. Priestley, (academic press, London, 1988), 237 pp. International

Journal of Forecasting 5, , 428 429.–

Cowen, R. K., Paris, C. B., & Srinivasan, A. (2006). Scaling of connecti vity in marine populations. , , 522 527.Science 311 –

de Paula Costa, M. D., Souza-Conceiç~ ao, J. M., Schwingel, P. R., &

Spach, H. L. (2011). Assessment of larval distribution of invasive Omobranchus punc tatus (Valenciennes, 1836)(Pisces: Blenniida e) in a

subtropical estuary (southern Brazil). , , S33 S38.Aquatic Invasions 6 –

Domingues, V. S., Bucciarelli, G., Almada, V. C., & Bernardi, G. (2005). His- torical colonization and demography of the Mediterranean damselfish,

Chromis chromis Molecular Ecology 14. , , 4051 4063.–

Domingues, V. S., Santos, R. S., Brito, A., Alexandrou, M., & Almada, V. C. (2007). Mitochondrial and nuclear markers reveal isolation by distance

and effects of Pleistocene glaciations in the northea stern Atlantic and

Mediterranean populations of the white seabream ( , .).Diplodus sargus L

Journal of Experimental Marine Biology and Ecol ogy 346, , 102 113.–

Domingues, V. S., Santos, R. S., Brito, A., & Almada, V. C. (2006). Historical

population dynamics and demogra phy of the eastern Atlantic pomacentrid (Valenciennes, 1833).Chromis limbata Molecular Phyloge-

netics and Evolution 40, , 139 147.–

Edwards, A. (1986). A new damselfish, (Teleostei:Chromis lubbocki

Pomacentridae) from the Cape Verde archipelago, with notes on other

eastern Atlantic pomacentrids. ,Zoologische Mededelingen 60 ,

181 207.–

Elith, J., & Leathwick, J. R. (2009). Species distribution mo dels: ec ological

explanation and prediction across space and time. Annual Review of

Ecology, Evolution, and Systematics 40, , 677 697.–

Elith, J., Phillips, S. J., Hastie, T., Dudík, M., Chee, Y. E., & Yates, C. J.

(2011). A statistical explanation of MAXENT for ecologists. Diversity

and Distributions 17, , 4 3–57. Farashi, A., & Naderi, M. (2017). Predicting invasion risk of raccoon Pro-

cyon lotor Landscape andin Iran using environmental niche models.

Ecological Engineering 13, , 229 236.–

Ferreira, C., Floeter, S., Gasparini, J., Ferreira, B., & Joyeu x, J. (2004a). Tro-

phic structur e patterns of Brazilian reef fishes: a latitudinal compari-

son. , , 1093 1106.Journal of Biogeography 31 –

Ferreira, C. E., Luiz, O. J., Floeter, S. R., Lucena, M. B., Barbosa, M. C.,

Rocha, C. R., & Rocha, L. A. (2015). First record of invasive lionfish

( ) for the Brazilian coast. , , e0123002.Pterois volitans PLoS One 10

Ferreira, C. E. L., Gonçalves, J. E. A., & Coutinho, R. (2004b). Cascos de

navios e plataformas como vetores na introdu ç~ ao de espécies exóticas.

Agua de lastro e bioinvas ~ ao 1, , 143 155.–

Ferreira, C. E. L., Junqueira, A. d. O. R., Villac, M. C., & Lopes, R. M. (2009).

Marine bioinvasion s in the Brazilia n coast: Brief report on history of

events, vectors, ecology, impacts and managem ent of non-indigenous species. In (pp. 459 477). Ber-Biological invasions in marine ecosystems –

lin, Heidelberg: Springer.

Floeter, S. R., Guimar~ aes, R. Z. P., Rocha, L. A., Ferreira, C. E. L., Rangel, C. A., & Gasparini, J. L. (2001). Geographic variation in reef-fish

assemblages along the Brazilian coast. Global Ecology and Biogeogra-

phy 10, , 423 431.–

Froese, R. & Pauly, D. (2019). Fishbase (www database). World Wide Web Electronic Publications . Retrieved from https://www.fis hbase.de/s-

earch.php (accessed June 2019).

G o l l a s c h , S . , L e n z , J . , D a m m e r , M . , & A n d r e s , H . - G . ( 2 0 0 0 ) . S u r v i v a l o f t r o p i c a l b a l l a s t w a t e r o r g a n i s m s d u r i n g a c r u i s e f r o m t h e I n d i a n

O c e a n t o t h e N o r t h S e a . J o u r n a l o f P l a n k t o n R e s e a r c h , ,2 2

9 2 3 9 3 7 .–

Graves, S., Piepho, H. & Selzer, L. (2015). Dorai-Raj S. multcompView: visu-

alizations of paired com parisons. , 01-05.R package version

Hernandez, P. A., Graham, C. H., Master, L. L., & Albert, D. L. (2006). The effect of sample size and species characteristics on performance of

different species distribution modeling methods. Ecography , ,29

773 785.–

Horta, P., Amancio, E., Coimbra, C., & Oliveira, E. (2001). Considerações

sobre a distribuiç~ ao e origem da flora de macroalgas marinhas

brasileiras. , , 243 265.Hoehnea 28 –

Hothorn, T., Bretz, F., Westfa ll, P., Heiberger, R. M., Schuetzenmeister, A.,

Scheibe, S., & Hothorn, M. T. (2016). Package multcomp. Simultan eous“ ”

inference in general parametric models. Vienna, Austria: Project for Sta- tistical Computing.

Johnston, M. W., & Purkis, S. J. (2016). Forecasting the success of invasive

marine species; lessons learned from purposeful reef fish releases in the Hawaiian islands. , , 190 200.Fisheries Research 174 –

Ka uch, P., Berggren, Å., & Cassel-Lundhagen, A. (2014). Genetic diversityň

of a succes sful colonizer: isolated populations of Metrioptera roeselii

regain variation at an unusually rapid rate. , ,Ecology and Evolution 4

1117 1126.–

Katsanevakis, S., Coll, M., Piroddi, C., Steenbeek, J., Ben Rais Lasram, F., Zenetos, A., & Cardoso, A. C. (2014). Invading the Mediterranean Sea:

biodiversity patterns shaped by human activities. Frontiers in Marine

Science 1, , 32. Kletou, D., Hall-Spencer, J. M., & Kleitou, P. (2016). A lionfish ( )Pte rois miles

invasion has begun in the Mediterranean Sea. Marine Biodiversity

Records 9, , 46. Laglbauer, B. J. L., Afonso, P., Donnay, A., Santos, R. S. & Fontes, J. (2017).

Reproductive synchrony in a temperate damselfish, Chromis limbata.

acta ethologica 20, 297-311. Leite, J. R., Bertoncini, A. A., Bueno, L., Daros, F., Alves, J., & Hostim-

Silva, M. (2009). The occurrence of Azores Chromis, inChromis limbata

the South-Western Atlantic. , , e145.Marine Biodiversity Record s 2

Lenth, R., & Lenth, M. R. (201 8). Package lsmeans. .“ ” The American Statisti-

cian 34, , 216 221.–

Lopes, R. M. C., Pombo, L., Cunha, V. B. & Rimoldi, D. (2009). Informe sobr e

as espécies exóticas invasoras marinhas no Brasil: Ministério do Meio

Ambiente, Brasília, Série Biodiversidade 33, 440 pp.

Luiz, O. J., Allen, A. P., Robertson, D. R., Floet er, S. R., & Madin, J. S. (2015). Seafarers or castaways: ecological traits associated with rafting

dispersal in tropical reef fishes. ,Journal of Biogeography 42,

2323 2333.–

Luiz, O. J., Floeter, S., Gasparini, J., Ferreira, C., & Wirtz, P. (2004). The

occurrence of (P erciformes: Acanthuridae) inAcanthurus monroviae

the South-Western Atlantic, with comments on other eastern Atlantic reef fishes occurring in Brazil. , , 1173 1179.Journal of Fish Biology 65 –

Luiz, O. J., Madin, J. S., Robertson, D. R., Rocha, L. A., Wirtz, P., &

Floeter, S. R. (2012). Ecolo gical traits influencing range expansion across large oceanic dispersal barrier s: insights from tropical Atlantic

reef fishes. Proceedings of the Royal Society of London B: Biological Sci-

ences 279, , 1033 1040.–

Mapstone, G. M., & Wood, E. M. (1975). The ethology of Abudefduf

luridus and (Pisces: Pomacentridae) from the Azores.Chromis chromis

Journal of Zoology 175, , 179 199.–

Matano, R. P., Palma, E. D., & Piola, A. R. (2010). The influence of the Brazil

and Malvinas currents on the southwestern Atlantic shelf circulation.

Ocean Science 6, , 983 995.–

372 ANDERSON .ET AL

FISH



Moura, R. L. d., Gasparini, J. L., & Sazima, I. (1999). New records and range extensions of reef fishes in the Western South Atlantic, with com-

ments on reef fish distribution along the Brazilian coast. Revista

Brasileira de Zoologia 16, , 513 530.–

Olson, D. B., Podestá, G. P., Evans, R. H. , & Brown, O. B. (1988). Temporal

variations in the separation of Brazil and Malvinas currents. Deep Sea

Research Part A Oceanograp hic Research Papers 35. , , 1971 1990.–

Schofield, P. J. (2009). Geographic extent and chronology of the invasion

of non-native lionfish ( (Linnaeus 1758) andPterois volitans P. miles

(Bennett 1828)) in the Western North Atlantic and Caribbean Sea. Aquatic Invasions 4, , 473 479.–

Pajuelo, J. G., González, J. A., Triay-Portella, R., Martín, J. A., Ruiz- Díaz, R.,

Lorenzo, J. M., & Luque,

A. (2016). Introduction of non-native marine fish species to the Canary Islands waters through oil platforms as vec-

tors. ,Journal of Marine Systems 163, 23– 30.

Pecl, G. T., Araújo, M. B., Bell, J. D., Blanchard, J., Bonebrake, T. C., Chen, I.-C., Williams, S. E. (2017). Biodiversity redistribution under…

climate change: impacts on ecosystems and human well-being. ,Science

355, eaai9214.Peliz, A., Dubert, J., Santos, A. M. P., Oliveira, P. B., & Le Cann, B. (2005).

Winter upper ocean circulation in the Western Iberian Basin-fronts,

eddies and poleward flows: an overview. Deep Sea Research Part I:

Oceanographic Research Papers 52, , 621 646.–

Philips, S. J., & Dudík, M. (2008). Modeling of species distributions with

Maxent: new extensions and a comprehensi ve evaluation. ,Ecography

31, 161 175.–

Phillips, S., Dudik, M. & Schapire, R. (2011). Maximum entropy modeling of

species geographic distr ibutions (MaxEnt), version 3.3. 3k. Pinheiro, H. T., Bernardi, G., Simon, T., Joyeux, J.-C., Macieira, R. M.,

Gasparini, J. L., Rocha, L. A. (2017). Island biogeography of marine…

organisms. ,Nature 549, 8 2–85. Pinnegar, J. (2018). Why the damselfish is a key species inChromis chromis

the Mediterranean rocky littoral a quantitative perspective.– Journal of

Fish Biology 92, , 851 872.–

Raventós, N., & Macpherson, E. (2001). Planktonic larval duration and set-

tlement marks on the otoliths of Mediterranean littoral fishes. Marine

Biology , , 1115 1120.138 –

Rencher, A. C., & Schaalje, G. B. (2008). (p. 678).Linear models in statistics

Hoboken, NJ: Published simultaneously in Canada.

Robertson, D. R., Simoes, N., Rodríguez, C. G., Piñeros, V. J., & Perez- España, H. (2016). An indo-Pacific damselfish well established in the

southern Gulf of Mexico: prospects for a wider, adverse invasion. Jour-

nal of the Ocean Science Foundation 19, , 1–17. R Core Team 2019: A Language and Environment for Statistical Comput-

ing R. Foundation for Statistical Computing, Vienna, Austria. https://

www.R-project.org/. Snedecor, G., & Cochran, W. (1989). The normal distribution. In Statistical

methods Io wa State University Press(8th ed., pp. 53 58). Ames, IA:– .

Tyberghein, L., Verbruggen, H., Pauly, K., Troupin, C., Mineur, F., & De Clerck, O. (2012). Bio-ORACLE: a global environmental dataset for

marine species distribution modelling. ,Global Ecology and Biogeography

21, 272 281.–

Underwood, A. (1981). Techniques of analysis of variance in experimental

marine biology and ecology. Oceanography and Marine Biology An

Annual Review 19, , 513 605.–

Verbruggen, H., Tyberghein, L., Pauly, K., Vlaeminck, C.,

Nieuwenhuyze, K. V., Koois tra, W. H. C. F., Clerck, O. D. (2009).…

Macroecology meets macroevolution: evolutionary niche dynamics in the seaweed Halimeda. , , 393 405.Global Ecology and Biogeogr aphy 18 –

Wanless, R. M., Scott, S., Sauer, W. H. H., Andrew, T. G., Glass, J. P.,

Godfrey, B., Yeld, E. (2010). Semi-submersible rigs: a vector…

transporting entire marine communities around the world. Biological

Invasions 12, , 2573 2583.–

Williams, R. J., Griffiths, F. B., Va n der Wal, E. J., & Kelly , J. (1988). Cargo vessel ballast water as a vector for the transport of non-indig enous

marine species. , , 409 420.Estuarine, Coastal and Shelf Science 26 –

Williamson, M., & Fitter, A. (1996). The varying success of invaders. Ecol-

ogy 77, , 1661 1666.–

Wilmsmeier, G., & Monios, J. (2016). Institutional structure and agency in

the governance of spatial diversification of port system evolution in Latin America. , , 294 307.Journal of Transport Geography 51 –

Wirtz, P. (2012). Seven ne w records of fish from NGor Island, Senegal.

Arquipelago Life and Marine Sciences 29, , 77 –81. Wonham, M. J., Carlton, J. T., Ruiz, G. M., & Smith, L. D. (2000). Fish and

ships: relating dispersal frequency to success in biological invasions.

Marine Biology 136, , 1111 1121.–

Wood, E. M. (1977). A review of dams el fishes (Pisces: Pomacentridae) of

the genus from the central and easte rn Atlantic and the Medi-Chromis

terranean. , , 331 345.Journal of Fish Biology 10 –

Zar, J. (1999). . Upper Saddle River, NJ: Prentice Hall.Biostat istical analysis

S U P P O R T I N G I N F O R M A T I O N

Additional supporting information may be found online in the

Supporting Information section.

How to cite this article: Anderson AB, da Silva JP, Sorvilo R,

Francini CLB, Floeter SR, Barreiros JP. Population expansion

of the invasive Pomacentridae (Valenciennes,Chromis limbata

1833) in southern Brazilian coast: long-term monitoring,

fundamental niche availability and new records. .J Fish Biol

2020;97:362 373.– https://doi.org/10.1111/jfb.14365




limbata ( V a l e n c i e n n e s , 1 8 3 3 ) i n s o u t ...

Documents

Transcript of limbata ( V a l e n c i e n n e s , 1 8 3 3 ) i n s o u t ...