Journal of Animal Ecology 2013, 82, 468–477
doi: 10.1111/j.1365-2656.2012.02034.x
Climate change exacerbates interspecific interactions
in sympatric coastal fishes
Marco Milazzo1*, Simone Mirto2, Paolo Domenici3 and Michele Gristina4
1
Department of Earth and Marine Sciences (DiSTeM), University of Palermo, Palermo, Italy; 2IAMC-CNR, Messina,
Italy; 3IAMC-CNR, Torregrande, OR, Italy; and 4IAMC-CNR, Mazara del Vallo, TP, Italy
Summary
1. Biological responses to warming are presently based on the assumption that species will
remain within their bioclimatic envelope as environmental conditions change. As a result,
changes in the relative abundance of several marine species have been documented over the
last decades. This suggests that warming may drive novel interspecific interactions to occur
(i.e. invasive vs. native species) or may intensify the strength of pre-existing ones (i.e. warm
vs. cold adapted). For mobile species, habitat relocation is a viable solution to track tolerable
conditions and reduce competitive costs, resulting in ‘winner’ species dominating the best
quality habitat at the expense of ‘loser’ species.
2. Here, we focus on the importance of warming in exacerbating interspecific interactions
between two sympatric fishes. We assessed the relocation response of the cool-water fish Coris
julis (a potential ‘loser’ species in warming scenarios) at increasing relative dominance of the
warm-water fish Thalassoma pavo (a ‘winner’ species). These wrasses are widespread in the
Mediterranean nearshore waters. C. julis tolerates cooler waters and is found throughout the
basin. T. pavo is common along southern coasts, although the species range is expanding
northwards as the Mediterranean warms.
3. We surveyed habitat patterns along a thermo-latitudinal gradient in the Western Mediterranean Sea and manipulated seawater temperature under two scenarios (present day vs.
projected) in outdoor arenas. Our results show that the cool-water species relocates to a lesspreferred seagrass habitat and undergoes lower behavioural performance in warmer environments, provided the relative dominance of its warm-water antagonist is high.
4. The results suggest that expected warming will act synergistically with increased relative
dominance of a warm-water species to cause a cool-water fish to relocate in a less-preferred
habitat within the same thermal environment.
5. Our study highlights the complexity of climate change effects and has broad implications
for predictive models of responses to warming. To achieve more accurate predictions, further
consideration is needed of the pervasive importance of species interactions. We believe these
fundamental issues to be addressed to understand the biotic consequences of climate change.
Key-words: behaviour, cold-adapted, competition, labrids, Mediterranean Sea, relocation,
global warming
Introduction
Empirical evidence suggests that climate warming should
favour warm-adapted species over cold-adapted species at
the same site (Parmesan & Yohe 2003). In some marine
regions, average sea surface temperatures (SST) have risen
faster than the global average (Trenberth et al. 2007) and
rapid poleward shifts of isotherms have been recorded
*Correspondence author.E-mail: [email protected]
(Burrows et al. 2011). Consequently, mass mortality
events, depth/latitudinal shifts and relative dominance
changes of several marine species have been well documented over the last decades (Perry et al. 2005; Sabatés
et al. 2006; Dulvy et al. 2008; Coma et al. 2009; Lejeusne
et al. 2009; Coll et al. 2010). Indeed, thermal sensitivity is
a fundamental physiological attribute and one principal
reason for climate-induced changes in natural communities
(Pörtner & Farrell 2008). Species coexist where their thermal windows overlap, although thermal windows may be
© 2012 The Authors. Journal of Animal Ecology © 2012 British Ecological Society
Warming effects and species interactions
not identical (Pörtner & Peck 2010). In turn, coexistence
may increase inter-specific interactions under warming
(Tylianakis et al. 2008) and these can modify the magnitude of species responses to climate change (Harley et al.
2006).
Hence, attributes other than fundamental temperaturerelated physiological processes (Pörtner & Farrell 2008)
may be evoked to further explain biotic changes (Gilman
et al. 2010). Although (i) species interactions are among
the most important forces structuring ecological communities; and (ii) information on how a changing climate
affects the extent of density changes is considered central
to building more accurate predictions, climate change
impacts on species distribution, biodiversity and ecosystem functioning are probably underestimated by current
forecasts mostly neglecting such processes (Harley et al.
2006; Tylianakis et al. 2008; Gilman et al. 2010).
At present, empirical evidence on the role of warming
in modulating the strength of species interactions is still in
its infancy (but see Helland et al. 2011; Harley 2011).
Given likely stability in overall species composition, documented changes in the relative dominance of species along
a thermal gradient (Simpson et al. 2011) are expected to
have a much greater impact on the ecology and exploitation of fish assemblages than any range extensions or contractions (Harborne & Mumby 2011), for example,
creating novel inter-specific interactions or exacerbating
pre-existing antagonistic ones (Gilman et al. 2010). Under
a warming scenario, local or regional relocations that
track tolerable conditions (Parmesan & Yohe 2003) and
reduce competitive costs (Parmesan 2006) are viable solutions for mobile species. This may result in ‘winner’ (i.e.
warm-adapted) species dominating the best quality habitat
at the expense of ‘loser’ (cold-adapted) species.
Here, we investigate (i) the thermo-latitudinal patterns
of habitat selection of a warm-water and a cool-water
species in several locations spanning 10° latitude in the
Western Mediterranean Sea and analyse (ii) the effects of
experimentally increasing the relative dominance of a
potential ‘winner’ species on the relocation and behavioural responses of its ‘loser’ antagonist, under present day
and projected SST by 2100 (Somot et al. 2008). We studied two ecologically and morphologically similar Atlantic–
Mediterranean coastal wrasses (Osteichthyes: Labridae).
Specifically, we tested the hypothesis that projected warming combined with higher relative dominance of the
warm-water fish will (i) displace the cool-water species
from the preferred habitat and (ii) alter its behaviour.
Materials and methods
study species and habitat use in the wild
We selected two sympatric coastal fish as species model: the rainbow wrasse Coris julis Linnaeus, 1758 and the ornate wrasse
Thalassoma pavo Linnaeus, 1758 (Fig. S1, Supporting information). These wrasses are among the most abundant and
469
widespread species in the Eastern Atlantic and the Mediterranean
Sea nearshore waters and have similar body size, habitat preference, feeding strategies and diets (Kabakasal 2001). C. julis tolerates cooler waters and is found throughout the Mediterranean
basin (Froese & Pauly 2011). T. pavo is more common in warmer
southern coasts (Froese & Pauly 2011), although it is expanding
northward as the Mediterranean warms (Lejeusne et al. 2009;
Coll et al. 2010) (see Supporting Information).
To assess the thermo-latitudinal patterns of habitat selection of
these wrasses, density of both species was estimated along replicated linear transects of 5 9 25 m (Harmelin-Vivien et al. 1985)
positioned at 3–10 m depth in uniform algal (Cystoseira spp. forest) and seagrass habitats (Posidonia oceanica meadow). Sampling
locations were located at four thermo-latitudinal levels crossing
the 14 °C February isotherm (~40°N), a long recognized biogeographical divide that several warm-water species (including
T. pavo) have crossed over the 25 years as the Mediterranean
have warmed (Bianchi 2007). To avoid any confounding from
other anthropogenic stressors (e.g. pollution and angling), within
each latitude level, two locations were randomly selected among
low-impacted, pristine and marine protected areas in the Sicily
Strait (~35°N), Southern Tyrrhenian Sea (~38°N), Central
Tyrrhenian Sea (~41°N) and Ligurian Sea (~44°N) (Fig. 1a). Two
random areas within each location were selected, and replicated
counts were performed in each site for the two species independently (see Experimental designs section), and then standardized
to 100 m2.
manipulative experiments in outdoor arenas
Individuals of both species were collected from three different
locations along the northern coast of Sicily (e.g. Messina Strait,
Ustica Island and Gulf of Carini). We choose to collect animals
from southern Mediterranean locations, thus potential differences
in the responses we searched for might be conservative, being animals adapted to a warmer average annual SST.
Hypotheses of habitat relocation and interspecific interactions
between the two wrasses species under two thermal scenarios
have been experimentally approached on a step-by-step base: 1.
the ‘single species’ and 2. the ‘relative dominance’ experiments.
All the individuals to be used for the manipulative experiments
(a total of 1620 T. pavo and 990 C. julis) were selected according
to their adult colour phases and total length (see Table S1,
Supporting information).
Under present-day and projected SST, a choice of different
artificial habitats was offered to independent groups of fifteen
individuals of both species separately (the ‘single species’ experiment) and to fifteen Coris julis individuals at increasing levels of
Thalassoma pavo relative dominance: 1X (fifteen T. pavo individuals, that is, both species in the same proportion), 2X (30 T. pavo
ind.) and 3X (45 T. pavo ind.). Size structure of each group of fifteen fishes was: two terminal phase males (80–180 mm total
length), eight intermediate initial phase females or sneaker males
(81–140 mm TL) and five small initial phase females (50–80 mm
TL) individuals for both species (Table S1, Supporting information). The ranges of abundance and size structure were based on
own field data, and experimental densities were standardized to
the arena surface. Before each experiment started, fish were acclimated to holding tanks under the same experimental conditions
of the outdoor arenas for 20 days (Supporting information). The
same individual was used only once within each thermal scenario,
© 2012 The Authors. Journal of Animal Ecology © 2012 British Ecological Society, Journal of Animal Ecology, 82, 468–477
470 M. Milazzo et al.
40
Algal habitat
(b)
26·5
(a)
26
30
25·5
25
20
24·5
24
23·5
23
0
10
Seagrass habitat
(c)
26·5
26
7·5
Summer SST (°C)
n. of ind. 100 m–2
10
25·5
25
5
24·5
24
2·5
23·5
0
23
44·14 44·01 40·55 40·53 38·42 38·30 35·85 35·30
Latitude (°N)
T. pavo
C. julis
SST 2005
Fig. 1. Habitat selection of the coastal wrasses in the Western Mediterranean Sea. (a) Sampling locations along the thermo-latitudinal
gradient (35°–44°N): Lampedusa Island (La) at 3530°N and Linosa Island (Li; 3585°N) in the Sicily Strait [winter surface seawater temperature (SSTw) was 147 ± 12 °C and the summer SST (SSTs) were 255 ± 09 °C]; Ustica (Us, 3842°N), Salina (Sa, 3830°N) (SSTw
144 ± 094 °C, SSTs 254 ± 13 °C), Tavolara (Ta, 4055°N) and Ponza (Po, 4055°N) (SSTw 136 ± 06 °C and SSTs 251 ± 11 °C) in
the Tyrrhenian Sea; Gallinara (Ga, 4401°N) and Palmaria (Pa, 4414°N) (SSTw 140 ± 06 °C and SSTs 236 ± 06 °C). (b–c) Mean
densities (±SE) of the two wrasse species and average summer SST (±SD) along the latitudinal gradient in the algal and the seagrass habitat, respectively. Note that the y-axis scale varies among plots.
whilst the same specimens were used for present-day and projected SST scenarios to avoid excessive collection of fish (Supporting information). Combinations of fish individuals of
different sizes among different thermal scenarios were randomly
chosen by capturing fishes from the holding tanks.
Average SST of the Mediterranean Sea have risen faster than
the global average (Trenberth et al. 2007), increasing by 066° C
in the Western part of the basin and by 11° C in the Levantine
basin over the past 20 years (Nykjaer 2009). As the Mediterranean Sea is constrained to the north by the European landmass
and its average SST are predicted to increase by a further 23–
26° C (Somot et al. 2008) or even by 31° C (Coll et al. 2010) by
the end of this century, biological responses to warming may be
dramatic in the near future. Therefore, rearing conditions in
small tanks and test conditions in two large outdoor arenas (8 m
diameter; 15 m depth; 50 m2 surface) were based on present-day
and on projected SST for 2100: a present-day scenario (Taverage
235 ± 07° C; Trange 218–244° C over the entire experiment)
ideal for both species and in the range of the temperature found
in the field, and a projected scenario (Taverage 282 ± 05° C;
Trange 271–288° C over the entire experiment) following
a + 27° C anomaly, relative to the average summer SST
recorded in SW Mediterranean (Somot et al. 2008). In warm and
sunny days, it was difficult to keep constant the seawater
temperature of the outdoor arenas. Therefore, we constantly
monitored temperature (and other abiotic parameters, see
Supporting information), and if values exceeded our desired
ranges, the experiment trials were stopped.
Different artificial habitats were provided to animals for the
choice experiments. The artificial macroalgae (Flowering
Cabomba, AquaPlant® Penn-Plax®, Memphis, TN, USA) mimicked the size (~35 cm high) and shape of Cystoseira spp., the most
common erect macroalgae in all study areas. The artificial seagrass
habitat mimicked the P. oceanica seagrass (Schofield 2003), a Mediterranean endemic species considered a key ecosystem in the
region (Hemminga & Duarte 2000); each shoot was made of green
plastic raffia, forming eight leaves of ~60 cm height and 08 cm
wide. Artificial macroalgae and seagrass shoots were placed
~25 cm apart, with approximately 500 mimics on a 25 m2 surface
of substrate. Bare plastic net substrate was also considered as artefact treatment (see experimental designs section and supplementary
information).
density and behavioural estimates in the
arenas
The density of C. julis was visually assessed and used as a proxy
of habitat selection both for the ‘single species’ and the ‘relative
dominance’ experiment. Observations occurred between 8:00 and
16:00 h, the peak activity period for wrasses (Willis,
Badalamenti & Milazzo 2006). Direct observations were made
from the arena border by a motionless operator, whose presence
© 2012 The Authors. Journal of Animal Ecology © 2012 British Ecological Society, Journal of Animal Ecology, 82, 468–477
Warming effects and species interactions
did not appear to disturb the fish. To avoid the observer bias,
three of us (M.M., S.M. and M.G.) haphazardly followed a
single individual separately, repeating observations three times
for each combination of treatments. A 3-min observation period
was used for recording habitat permanence and the other
behavioural activities only when the fish was inside the selected
habitat in the pairwise choice (Supporting information). The following behaviours of C. julis were quantified: (i) searching (i.e.
swimming close to and looking at the substrate); (ii) resting (i.e.
remaining motionless over the substrate); (iii) interacting with
cospecifics (swimming near cospecifics or exhibiting interactions
with other C. julis individuals); and (iv) interacting with T. pavo
(swimming near or exhibiting antagonist interactions with
T. pavo individuals). Habitat permanence and behavioural activities were expressed as the percentage of time spent in the selected
habitat upon the observation period.
Each trial consisted of a single replicate for density estimates
(i.e. counts were repeated three times at randomly chosen 10-min
intervals and their average was treated as a single replicate; a
total of three replicates were considered for each combination)
and three replicated habitat permanence and behavioural observations of C. julis individuals of different size classes. Individuals
were haphazardly selected from each arena for observations: one
terminal phase male, one intermediate initial phase and one small
initial phase female for each trial. A total of nine replicates were
considered for each combination. After the experiment, fish were
removed from arenas using hand nets or traps and released in the
holding tanks.
experimental designs and statistical
analyses
To assess patterns of habitat selection of the two wrasses in the
wild, a five-way design was conducted including the following
factors (and treatments): ‘Species’ (SP: C. julis and T. pavo), ‘Latitude’ (LA: 44°-41°-38°-35°N), ‘Habitat’ (HA: Algae vs. Posidonia
seagrass), ‘Location’ (LO: two levels) and ‘Area’ (AR: two levels).
Four random density replicates (individuals 100 m 2) were considered for each combination of the above treatments (N = 256)
(Fig. S2, Supporting information).
A preliminary ‘single species’ experiment was performed to
assess the most preferred artificial habitat by each fish species
separately. Trials consisted of single species at 1X density (15
individuals) released within arenas. The factors involved were
Habitat (HT: A9S, S9A), Thermal scenarios (TS: present day
and projected) and Arena (A1 and A2). The number of individuals 25 m 2 at each combination of treatments was visually
assessed and used as surrogate of habitat selection for C. julis
and T. pavo separately. A total of three density replicates were
collected (N = 24) (Fig. S3, Supporting information).
To evaluate the relocation response of the cool-water fish to
increasing relative dominance of the warm-water fish at two distinct temperature scenarios, a pairwise choice of combinations of
two habitats (algae and seagrasses) and of an appropriate artefact
control (i.e. the plastic net substrate) was provided to fish in large
outdoor arenas. In this case, the experimental design consisted of
three factors: ‘Temperature scenario’ (TS: C as Present day and
W as Projected SST); ‘T. pavo density’ (DT: 1X, 2X, 3X of
C. julis density); ‘Habitat’ (HT) with six levels resulting from independent combinations of Algae + Net (A), Seagrass + Net (S)
and Net substrate (N): A9S, A9N, S9A, S9N, N9A, N9S.
471
A total of three density replicates (no. of individuals 25 m 2)
were collected (N = 108) to assess the relocation response of the
cool-water C. julis, and a total of nine replicates were considered
for each combination (N = 324) to assess its habitat permanence
(Time%) and the behavioural responses (Time%) (Fig. S4, Supporting information).
To avoid pseudoreplication, observations were independently
carried out on different combinations of pairwise choices of habitats provided to both species in the ‘single species’ experiment
and to the cool-water fish in the ‘relative dominance’ experiment.
The A9S treatment indicates that algae is the observed habitat in
the pairwise choice algae vs. seagrass, whilst in the S9A treatment observations were conducted on the seagrass habitat. Each
day, the combinations of factors’ treatments (Figs S3–S4, Supporting information) were randomly assigned to two arenas and
each replicate of the same combination was collected on different
days. Moreover, habitat substrata were randomly positioned/oriented within arenas (Fig. S5, Supporting information).
Linear regression analyses were used to assess the relationships
between SST along the latitudinal gradient and the T. pavo and
C. julis density in the two shallow habitats separately. Five- and
three-way ANOVAs were used to test for species differences in the
patterns of habitat selection along the thermo-latitudinal gradient, habitat preference in the ‘single species’ experiment and the
habitat relocation, habitat permanence and behavioural activities
of the cool-water species in the ‘relative dominance’ experiment.
Cochran’s test was used to check for the homogeneity of variances. Significant interaction terms were examined individually
using Student–Newman–Keuls (SNK) a posteriori pairwise tests
to separate means at P = 005 (Underwood 1997).
Results
correlative field patterns of habitat
selection in the western mediterranean sea
From cooler to warmer locations (44°N-35°N), a shift in
the dominance of species was observed in the preferred
algal habitat (Fig. 1b; ANOVA: interaction term
SP9LA9HA F3,255 = 2918, P < 001; Table S2,
Supporting information) with C. julis being more
abundant than T. pavo at northern latitudes and the
opposite occurring at southern latitudes (Table 1). As
expected, the density of the cool-water C. julis in the algal
habitat was negatively correlated to the summer
(b = 116; r = 0899, P < 001; n = 8) and the winter
SST (b = 223; r = 0931, P < 0001; n = 8), whilst the
warm-water T. pavo density was positively correlated to
summer SST (b = 134; r = 0837, P < 001) and winter
SST (b = 284; r = 0955, P < 0001; n = 8). The shallow
seagrass beds at 38° and 35°N were increasingly occupied
by the cool-water wrasse (Fig. 1c; Table 1; Table S2, Supporting information), and despite its affinity to cooler
temperatures, its density was positively correlated to summer SST (b = 14; r = 0756, P < 005) and to winter SST
(b = 26; r = 0779, P < 005; n = 8). Few individuals of
T. pavo were recorded in the seagrass habitat – even
where its density on the preferred algal habitat was high
(Fig. 1b,c; Table 1) – and no correlation with either
© 2012 The Authors. Journal of Animal Ecology © 2012 British Ecological Society, Journal of Animal Ecology, 82, 468–477
472 M. Milazzo et al.
summer or winter SST was observed (summer SST:
b = 01; r = 0612, P > 005; winter SST: b = 02;
r = 0450, P > 005; n = 8).
manipulative experiments in large outdoor
arenas
In the preliminary ‘single species’ experiment, the
warm-water Thalassoma pavo and the cool-water Coris julis exhibited similar patterns of habitat selection, with a
higher preference for the algal habitat than the seagrass
one
(C. julis
F1,24 = 2301,
P < 0001,
T. pavo
F1,24 = 4349, P < 0001; SNK tests: Algae > Seagrass for
both species at P < 005). This finding confirms the
patterns observed in the field; however, the thermal scenario per se slightly affected the selection of C. julis
(F1,24 = 492, P < 005; SNK test: Cool > Warm), and no
differences were detected in the interaction Habitat x
Thermal scenario (C. julis F1,24 = 004, P > 005, T. pavo
F1,24 = 232, P > 005). Moreover, the single species
experiments did not reveal any effect of the arena either
in the T. pavo or in the C. julis trials (F1,24 = 092,
P > 005, T. pavo F1,24 = 006, P > 005).
The potential interactions between the two wrasses were
further examined in the ‘relative dominance’ experiment. If
in these trials the cool-water C. julis retained the habitat
preferences exhibited in the ‘single species’ experiment, the
two species would largely overlap in habitat. This was not
Table 1. Summary of the results of the Student–Newman–Keuls post hoc tests. Only significant interaction terms at (P < 005) are
reported
Habitat selection (n. ind. 100 m 2) in the field patterns – Interaction term SP9LA9HA (Table S2, Supporting information)
44°: Algae (Cj > Tp). 41°: Algae (Cj > Tp). 38°: Algae (Tp > Cj), Seagrass (Cj > Tp). 35°: Algae (Tp > Cj), Seagrass (Cj > Tp)
Seagrass: Coris julis (35° = 38° = 41° > 44°). Algae: Thalassoma pavo (35° = 38° = 41° > 44°)
Coris julis: 41° (Al > Se), 44°(Al > Se). Thalassoma pavo: 35° (Al > Se), 38° (Al > Se), 41° (Al > Se)
Habitat selection (n. ind. 25 m 2) in the ‘relative dominance’ experiment – Interaction term TS9DT9HT (Table S3, Supporting
information)
1X: A9N (W > C), S9N (W > C), N9A (C > W), N9S (C > W). 2X: S9A (W > C). 3X: A9S (C > W), S9A (W > C)
Projected: A9S (1X > 2X = 3X), S9A (3X = 2X > 1X), S9N (1X > 2X = 3X)
3X: Projected (S9A > A9S = A9N = S9N = N9A = N9S)
Habitat permanence (% time) in the ‘relative dominance’ experiment – Interaction term TS9DT9HT (Table S3, Supporting
information)
1X: A9S (W > C), A9N (W > C), S9N (C > W), N9A (C > W), N9S (W > C). 2X: S9A (W > C), S9N (W > C). 3X: S9A
(W > C)
Projected: A9S (1X > 2X = 3X), A9N (1X > 2X = 3X), S9A (3X = 2X > 1X), S9N (3X = 2X > 1X), N9A (3X = 2X > 1X), N9S
(1X > 2X = 3X)
1X: Projected (A9N = N9S > A9S = S9A > S9N = N9A). 3X: Projected (S9A > A9S = A9N = S9N = N9A = N9S)
Searching (% time) in the ‘relative dominance’ experiment – Interaction terms TS9HT and TS9DT (Table S4, Supporting information)
TS9HT interaction term
N9A (C > W)
TS9DT interaction term
2X: (C > W). 3X: (C > W)
Resting (% time) in the ‘relative dominance’ experiment – Interaction term TS9DT9HT (Table S4, Supporting information)
1X: A9N (W > C), N9S (W > C). 2X: S9A (W > C). 3X: A9N (W > C), S9A (W > C), S9N (W > C)
Present day: A9S (1X > 2X = 3X). Projected: A9N (3X > 1X > 2X), S9A (3X = 2X > 1X), S9N (3X > 2X = 1X), N9S
(1X > 2X = 3X)
1X: Projected (N9S > A9N > S9N = N9A = A9S = S9A). 2X: Projected (S9A > A9S = S9N = N9A = N9S = A9N).
3X: Projected (S9A = S9N = A9N > A9S = N9A = N9S)
Interacting with C. julis (% time) in the ‘relative dominance’ experiment – Interaction term TS9DT9HT (Table S4, Supporting
information)
1X: A9S (C > W), A9N (W > C), S9A (C > W), N9A (C > W). 2X: A9N (W > C), S9N (W > C), N9A (W > C).
Present day: A9S (1X > 2X = 3X).
Projected: S9N (2X > 1X = 3X), N9A (2X > 1X = 3X)
2X: Projected (S9N > A9S = S9A = A9N = N9A = N9S)
Interacting with T. pavo (% time) in the ‘relative dominance’ experiment – Interaction term TS9HT and term DT (Table S4,
Supporting information)
TS9HT interaction term
N9A (W > C)
DT term
3X > 1X = 2X
Cj = Coris julis, Tp = Thalassoma pavo, Al = Algae; Se = Seagrass, Latitudes: 44°-41°-38°-35°N. 1X, 2X and 3X are the relative
dominance treatments of the warm-water species, W = projected warming scenario, C = cooler present-day scenario, A = algae with net
substrate, S = seagrass with net substrate, N = net substrate without algae or seagrass.
© 2012 The Authors. Journal of Animal Ecology © 2012 British Ecological Society, Journal of Animal Ecology, 82, 468–477
Warming effects and species interactions
15
(a)
1X relative dominance
100
(a)
1X relative dominance
(b)
2X relative dominance
(c)
3X relative dominance
75
50
25
0
100
75
Time %
the case even in the present-day scenario, where the coolwater fish showed no selection of any habitat regardless of
increasing relative dominance of the warm-water fish
(Fig. 2a–c; Table 1; Table S3, Supporting information) and
no differences were revealed in the habitat permanence
(Fig. 3a–c; Table 1; Table S3, Supporting information).
Searching over the substrate by the cool-water fish was the
main behaviour under the present-day SST scenario, particularly at 2X and 3X relative dominance of the warm-water
antagonist. Under this thermal scenario, resting activity of
C. julis was higher at the lowest relative dominance level
(1X) of T. pavo (Fig. 4a; Table 1; Table S4, Supporting
information). Under projected warming, the cool-water
wrasses shifted from algae to seagrass only when the relative dominance of the warm-water fish was 3X (Fig. 2c;
Table 1; Table S3, Supporting information). Accordingly,
C. julis spent a larger proportion of permanence time (%)
in the less-preferred habitat (Fig. 3c; Table 1; Table S3,
Supporting information), showing decreased searching
activity and increased resting underneath seagrass leaves
(Fig. 4a,c; Table 1; Table S4, Supporting information).
473
50
25
0
100
*
75
50
10
25
5
0
Present-day
Algae
0
n. of ind. 25 m–2
15
(b)
2X relative dominance
10
Projected
Seagrass
Fig. 3. Mean habitat permanence (time%) of Coris julis in the
pairwise choices of the algal and the seagrass habitats at increasing relative dominance (1X, 2X and 3X) of Thalassoma pavo
under the two temperature scenarios. ‘*’P < 005. ANOVA and
SNK test full results are reported in text and in Tables 1 and S3
(Supporting information).
5
0
15
(c)
3X relative dominance
*
10
5
0
Present-day
Algae
Projected
Seagrass
Fig. 2. Relocation response of the cool-water species. Mean density (±SE) of Coris julis in the independent pairwise choices of
the A9S (i.e. the algal habitat was observed) and S9A (the seagrass habitat was observed) at increasing relative dominance (1X,
2X and 3X) of Thalassoma pavo under the two temperature scenarios. ‘*’P < 005. ANOVA and SNK test full results are reported
in the text and in Tables 1 and S3, Supporting information.
Searching activity was significantly lower in the projected
than the present-day scenario, particularly at 2X and 3X
relative dominance of the warm-water fish (Fig. 4a;
Table 1; Table S4, Supporting information). No clear pattern was observed in the time (%) spent by C. julis interacting with conspecifics, although higher time (%) was
recorded in the algal habitat only at 1X density of T. pavo
(Fig. 4b; Table 1; Table S4, Supporting information).
Interspecific interactions (time%) of the cool-water fish
were significantly higher at 3X density of the warm-water
wrasse, independently to the thermal scenario (Fig. 4d;
Table 1; Table S4, Supporting information). The resting
activity of the cool-water fish significantly differed under
the present-day scenario only at 1X relative dominance of
the warm-water T. pavo (Fig. 4c; Table 1; Table S4, Supporting information), whilst resting in the seagrass habitat
was the dominant behaviour at 2X and 3X of T. pavo
relative dominance in the projected SST condition (Fig. 4c;
Table 1; Table S4, Supporting information).
© 2012 The Authors. Journal of Animal Ecology © 2012 British Ecological Society, Journal of Animal Ecology, 82, 468–477
474 M. Milazzo et al.
Time %
50
Searching activity
(a)
50
40
40
30
30
20
20
10
10
0
50
Interacting with co-specifics
(d)
Interacting with warm-water fish
0
(c)
50
Resting activity
40
40
30
30
20
20
10
10
0
(b)
Algae
Seagrass
Present-day
Algae
Seagrass
0
Algae
Projected
1X relative dominance
Seagrass
Algae
Present-day
2X relative dominance
Seagrass
Projected
3X relative dominance
Fig. 4. Behavioural response of the cool-water species. Behavioural activities of Coris julis (time% spent searching, resting, interacting
with co-specifics and interacting with Thalassoma pavo) in the pairwise choices of the algal and the seagrass habitats at increasing relative
dominance (1X, 2X and 3X) of T. pavo under the two thermal scenarios. ANOVA and SNK test full results are reported in text and in
Tables 1 and S4 (Supporting information). Note that behavioural activities occur within habitat permanence (Fig. 3).
Discussion
Here, we show the role of warming in exacerbating interspecific interactions between two ecological antagonists,
suggesting that anthropogenic climate change can alter
interspecific interactions and produce unexpected changes
in species distributions among habitats, potentially affecting community structure and diversity. More broadly, our
results on a two species model highlight the importance of
incorporating interspecific interactions into projections
regarding ecological responses to climate change.
Using correlative and experimental approaches, our
results showed that higher temperatures and relative dominance increase of a warm-water species may act synergistically causing a cool-water species (i) to relocate to a lesspreferred habitat within the same thermal environment;
and (ii) to alter its behavioural activity. However,
responses to seawater warming only took place when the
dominance of the warm-water fish was high, both in the
field study and in the experimental trials. In the most
southern and warmer locations of the thermo-latitudinal
gradient examined, we recorded the habitat relocation of
the cool-water fish to the seagrass meadows when the density of its warm-water antagonist in the preferred algal
habitat was from 5 to 7 times higher (particularly at 35°N).
Our manipulative experiments did support the observed
field patterns, highlighting that the ecological and behavioural responses of the cool-water C. julis are affected by
projected warming, provided the relative dominance of its
warm-water antagonist T. pavo was 3-fold higher. No such
effects are recorded in the present-day scenario.
Habitat relocation is a viable solution for interacting
species and often results in a characteristic distribution of
individuals among habitats. This should result in ‘winner’
warm-adapted species dominating the best quality habitat
with lots of individuals, whilst the ‘loser’ cold-adapted
species maintains fewer individuals, if it is present at all
(Tokeshi 1999). Indeed, the observed ability of C. julis to
modify its habitat selection according to the increasing
relative dominance of T. pavo is an important response,
which reduces habitat overlap, related ecological costs
and probably allows for coexistence in heterogeneous seabeds. Posidonia oceanica meadows might be regarded as a
suboptimal habitat, underused by T. pavo and representing a ‘refuge’ for C. julis where this species can avoid
potential detrimental inter-specific effects when its normally preferred habitat is occupied by the dominant
antagonist T. pavo. Similarly, a marked vertical shift in
sloping algal seabeds was recently observed, with C. julis
expanding to deeper and cooler environments when the
relative dominance of T. pavo was high in the warmer
and shallow water algal habitat, and the two species coexisting in slowly sloping algal seabeds (Milazzo et al.
2011). Both species swim close to the substrate and are
visual predators of invertebrates, and a strong association
with rocky algal assemblages is likely due to foraging
(Kabakasal 2001). Their small invertebrate preys live on
or under the algal canopy in the Cystoseira forest
(Chemello & Milazzo 2002), whilst in seagrasses, benthic
preys are concentrated in rhizomes and matte layers,
which are not easily accessible to these wrasses (Hemminga & Duarte 2000). Accordingly, previous studies
© 2012 The Authors. Journal of Animal Ecology © 2012 British Ecological Society, Journal of Animal Ecology, 82, 468–477
Warming effects and species interactions
showed that T. pavo is rare in seagrass beds whilst C. julis
is more commonly associated with this habitat and detects
prey along its edges particularly when the meadows are
fragmented (Vega-Fernandez et al. 2005). If in one hand,
the observed displacement of the cool-water species to the
Posidonia oceanica habitat is a viable solution to reduce
ecological costs, on the other an increasing habitat use of
C. julis in the seagrass meadows may cascade on other
community components (e.g. several other resident wrasse
species) potentially causing a rearrangement of the entire
community structure and functioning. However, projected
trajectories of P. oceanica persistence under forecasted
seawater warming in the Western Mediterranean demonstrate that the seagrass density may be affected by climate
change in the near future, possibly reaching a density
threshold below which meadow functionality is lost by
year 2049 (Jordà, Marbà & Duarte 2012). Although the
cool-water wrasse species may potentially benefit by a
lower P. oceanica seagrass density (Vega-Fernandez et al.
2005), whether and how its ecological performance will be
affected in the long term is presently unknown.
The cool-water fish showed decreased searching activity
under projected warming and increased resting in the lesspreferred seagrass habitat when its ecological antagonist
was on patrol at 2X and 3X relative dominance. As
expected, we also recorded increased interspecific interactions at 3X relative dominance of the warm-water fish,
independently to the thermal scenario considered. When
these interspecific interactions occurred under projected
warming, they were likely to cause behavioural changes in
the cool-water species. Interspecific behavioural interactions between wrasses, considered an essential part of
their ability to coexist (Jones 2002), mainly consisted of
the cool-water species readily forming hetero-specific
groups with several warm-water individuals (i.e. the swimming with T. pavo behaviour). This kind of behavioural
interaction was made up by individuals of C. julis starting
to swim faster or to exhibiting antagonist interactions
with T. pavo individuals. Although a low number of
aggressive encounters between wrasses have been
observed, we noticed this behaviour to cause evident alterations (i.e. decrease in searching activity and increase in
resting activity in the less-preferred habitat at 2X and 3X
density of T. pavo) to the cool-water fish under the projected scenario. We explain the observed lower performance of the cool-water wrasse as a result of these
interspecific behavioural interactions. In general, animals
can compete either by reducing the availability of a
shared resource to other animals (exploitation competition) or by reducing the ability of other animals to make
use of a shared resource through behavioural interactions
(interference competition) (e.g. Tokeshi 1999). Therefore,
our findings suggest that the habitat segregation between
T. pavo and C. julis is essentially an interactive segregation with species showing behavioural interactions and
warming playing a key role in the activity pattern and in
the relocation response of the cool-water species to the
475
less-preferred seagrass habitat. Temperature is known to
be a fundamental factor in controlling fish metabolic
scope (Fry 1971). Hence, the lower ecological and
behavioural performance of the cool-water species at projected warming conditions may be due to a decrease in its
metabolic capacity (aerobic scope, i.e. the metabolic confines within which any energy-demanding activity in
excess of basal metabolic rate must be undertaken) (Fry
1971) that occurred when its ecological antagonist was
highly dominant. Accordingly, it was recently demonstrated that competitive interactions between two salmonid fishes resulted in contrasting performance during
simulated winter conditions of ice-covered lakes (higher
darkness and lower temperatures), whilst a decreasing ice
cover with warmer temperatures may reverse this situation
(Helland et al. 2011).
Present predictions concerning biological responses to
warming are largely based on the assumption that these
species will remain within their bioclimatic envelope as
environmental conditions change (Parmesan & Yohe
2003; Guisan & Thuiller 2005). Therefore, information
on the direct effects of seawater warming on temperate
cool-adapted species (i.e. species range contractions and
deepening to track more favourable conditions) has
increased over the last decades (e.g. Perry et al. 2005;
Dulvy et al. 2008; Simpson et al. 2011). However, studies
aimed at investigating the responses of cool-water species
to novel inter specific interactions or to exacerbated preexisting interactions with warm-water species are largely
lacking or have been only hypothesized (Sabatés et al.
2006).
Our results provided insight into the importance of
warming and interspecific interactions in affecting the
patterns of distribution of species among shallow habitats, thus contributing to filling an information gap
(Harley et al. 2006). Habitat suitability models (HSMs)
applied to Mediterranean endemic fish assemblages demonstrated that by the end of the 21st century, the coldest
areas of the Mediterranean Sea (the Adriatic Sea, the
Ligurian Sea and the Gulf of Lion) are projected to
become a geographical ‘trap’ that would drive cool-water
endemic fish species towards extinction if projected
warming occurs (Ben-Rais Lasram et al. 2010). These
findings might even be conservative as models do not
take into consideration that other forcing biotic factors
can enhance direct warming effects (Ben-Rais Lasram
et al. 2010). We suggest that the complex ecological consequences of climate change can only be accurately
anticipated if we are able to understand the ways in
which biotic and abiotic factors interact. This knowledge
is critical to achieve more accurate predictions of
responses to climate change (Gilman et al. 2010). Therefore, important future challenges in studies of climateinduced ecological responses should take into account
the pervasive importance of interactions between ecologically similar species (i.e. cold vs. warm adapted, native
vs. invasive) and increase our knowledge on food web
© 2012 The Authors. Journal of Animal Ecology © 2012 British Ecological Society, Journal of Animal Ecology, 82, 468–477
476 M. Milazzo et al.
interactions and on the role of other drivers of density
change (e.g. habitat degradation, overfishing, pollution,
ocean acidification). We believe more detailed models
may be needed to adequately account for the effects of
interspecific interactions when predicting the distribution
and abundance of species under warming, the related
community- and ecosystem-level responses.
Acknowledgements
We thank E. Azzurro, L. Genovese, G. Maricchiolo and the staff at
IAMC-CNR at Messina (Italy) for helping in different ways and for technical assistance during experiments. We also thank A. Palmeri, I. Anastasi,
A. Procter and F. Quattrocchi for participation in the field and experimental studies. All animal experiments were carried out according to national
regulations for the treatment and welfare of experimental animals. The
study was supported by the EU Cost Action ‘Conservation Physiology of
Marine Fishes’ (FA1004). M.M. was partially supported by the EU ‘Mediterranean Sea Acidification under a changing climate’ project (MedSeA;
grant agreement 265103). The funders had no role in study design, data
collection and analysis, decision to publish or preparation of the manuscript. AVHRR Pathfinder Version 5 SST data were obtained from
NOAA/NESDIS/NODC and the University of Miami at http://las.pfeg.
noaa.gov/oceanWatch/oceanwatch.safari.php.
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© 2012 The Authors. Journal of Animal Ecology © 2012 British Ecological Society, Journal of Animal Ecology, 82, 468–477
Warming effects and species interactions
Received 23 March 2012; accepted 1 August 2012
Handling Editor: Martin Genner
477
to colour phases and relative size structure. Note that the same
individuals were used for the present-day and the projected SST
treatments to avoid excessive collection of fish.
Supporting Information
Additional Supporting Information may be found in the online version
of this article.
Fig. S1. The Two Wrasses Species. Terminal phase males of the
warm-water T. pavo (a) and the cool-water C. julis (c). Initial
phase individuals of T. pavo (b) and C. julis (d) respectively.
Fig. S2. Details of the experimental design adopted for the field
patterns of habitat selection.
Fig. S3. Details of the experimental design adopted for the ‘single
species’ experiment.
Fig. S4. Details of the experimental design adopted for the ‘relative
dominance’ experiment.
Fig. S5. The two outdoor arenas (in black) used for the manipulative experiments at the IAMC-CNR, Messina (Italy). Both
arenas have similar size: 8 m diameter, 1.5 m depth, and ~50 m2
surface.
Table S1. Number of individuals of both species used in the ‘single
species’ and the ‘relative dominance’ experiments divided according
Table S2. ANOVA on the density of the wrasses in two shallow
habitats (algae and seagrass) at four latitudes. ns not significant, *
P < 0.05, ** P < 0.01, *** P < 0.001. In bold the significant
interaction further examined by post-hoc SNK test (Table 1).
Table S3. ANOVA on the habitat selection and habitat permanence of
the cool-water fish in the relative dominance experiment. ns not
significant, **P < 0.01, ***P < 0.001. In bold the significant
interactions further examined by post-hoc SNK tests (Table 1).
Table S4. ANOVA on the searching, interacting with co-specifics (Cj),
interacting with T. pavo (Tp) and resting activities of the cool-water
fish in the relative dominance experiment. ns not significant,
*P < 0.05, **P < 0.01, ***P < 0.001. In bold the significant
interactions further examined by post-hoc SNK tests (Table 1).
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© 2012 The Authors. Journal of Animal Ecology © 2012 British Ecological Society, Journal of Animal Ecology, 82, 468–477