Post on 22-Oct-2021
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: aabbiologia@gmail.com;sergio.floeter@ufsc.br
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
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os Acores - 193.136.242.241 - /doi/epdf/10.1111/jfb.14365] at [24/09/2020].
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
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(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
ANDERSON .ET AL 365FISH
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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
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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.
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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)
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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,
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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.
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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
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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
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os Acores - 193.136.242.241 - /doi/epdf/10.1111/jfb.14365] at [24/09/2020].