efecto de uv en girella

JFB
Journal Name
jfb_12566
Manuscript No.
B
Dispatch: November 1, 2014
Author Received:
Journal: JFB
No of pages: 10
CE: Kalaiarasu
TS: REKHA
Journal of Fish Biology (2014) 0, 0–0
doi:10.1111/jfb.12566, available online at wileyonlinelibrary.com
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BRIEF COMMUNICATION
Effect of UV radiation on habitat selection by Girella
laevifrons and Graus nigra
J. Pulgar*†, P. Lagos*, D. Maturana*, M. Valdés*, M. Aldana‡
and V. M. Pulgar§
*Departamento de Ecología and Biodiversidad, República 470, Piso 3, Facultad de Ecologíay
Recursos Naturales, Universidad Andres Bello, Santiago, Chile, ‡Escuela de Pedagogía en
Biología y Ciencias, Facultad de Ciencia de la Educación, Santa Isabel 1278, Universidad
Central de Chile Santiago, Santiago, Chile and §Center for Research in Obstetrics &
Gynecology, Wake Forest School of Medicine and Biomedical Research Infrastructure Center,
Winston-Salem State University, Winston-Salem, NC 27110, U.S.A.
(Received 10 January 2014, Accepted 26 September 2014)
The effect of UV radiation on habitat use of two species of intertidal fishes that inhabit the same
pools but exhibit different activity levels and diets was measured: the highly active omnivorous Girella
laevifrons and the cryptic carnivorous Graus nigra. Individuals of each species were acclimated to a
tank divided in three sections with different illumination; no light (N/L), ultraviolet light (UV) and
white light (WL), and the time spent and number of visits to each section were recorded. Although
both species preferred the N/L section, G. laevifrons spent more time in UV and less time in WL
compared with G. nigra; G. laevifrons also displayed higher number of visits to UV, suggesting a
different tendency in space use in response to UV exposure in intertidal fishes.
© 2014 The Fisheries Society of the British Isles
Key words: behavioural response; environmental stressors; intertidal fishes.
In aquatic systems, the direct deleterious effects of ultraviolet radiation (UV) on planktonic organisms, primary production of dissolved organic matter (Tadetti & Sempéré,
2006), photosynthetic capacity of algae (Helbling et al., 1992; Watkins et al., 2001)
and the growth, abundance and survival of invertebrates and vertebrates (Jokiel & York,
1984; Bothwell et al., 1994; Kiffney et al., 1997; McNamara & Hill, 1999; Zamzow,
2003; Häder et al., 2011; Nava et al., 2011) have been well-documented. Evidence
shows that UV radiation affects all components of aquatic trophic webs from primary
producers to consumers (Häder et al., 2003); however, the effects of UV radiation on
intertidal organisms are largely unknown.
In the intertidal system, animals encounter a variety of environmental stressors,
such as high light levels, variable temperatures and salinities, desiccation, nutrient
limitations, wave exposure and high levels of radiation (Dayton, 1971; Sousa, 1979;
†Author to whom correspondence should be addressed. Tel.: + 56 02 6618416; email: [email protected]
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© 2014 The Fisheries Society of the British Isles
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J . P U L G A R E T A L.
Gosselin & Chia, 1995; Pulgar et al., 2013; Lamb et al., 2014). The effect of abiotic
variables, such as thermal variability and CO2 levels, on intertidal organisms has
previously been reported (Pulgar et al., 2005, 2006, 2007; Hofmann et al., 2012;
Navarrete et al., 2012). This is especially relevant for intertidal fishes, one of the
least-studied groups of organisms in the rocky intertidal zone. Recently, mechanisms
of tolerance to oxidative stress after UV exposure, including high antioxidant capacity,
were reported for some intertidal fishes (Carrasco-Malio et al., 2014), supporting the
potential effect of UV exposure on habitat selection in these species.
Intertidal fishes inhabit tide pools, which are spatially and temporally discrete habitats where significant variations in temperature, oxygen concentration and salinity are
observed (Metaxas & Scheibling, 1993, 1994; Bridges, 1994; Little & Kitching, 1996).
The physical variability of a tide pool depends principally on the tide pool’s location
within the intertidal vertical gradient, which determines the time during which the tide
pool will be isolated from the rest of the subtidal zone (Pulgar et al., 2007). The two
species studied, the omnivorous Girella laevifrons (Tshudi 1846) (Kyphosidae) and the
carnivorous Graus nigra Philippi 1987, showed higher abundance in high tide pools,
sectors most distal from the subtidal zone, during the early stages of their development
(Pulgar et al., 2006).
High intertidal zones show great variability in physical variables that have been indicated as determinant factors in the distribution and abundance of species (Paine, 1977).
Therefore, the present study species are continuously exposed to high physical variability, including UV radiation. The study of the effect of UV exposure on organisms is
particularly necessary in countries such as Chile, where the highest increase in UV
radiation has been reported (Wahl et al., 2004). Moreover, these studies can help to
reveal survival strategies of organisms to UV stress and thus add to the understanding of
the effects of ongoing climate change (Hughes, 2000). Although, both studied species
inhabit the same pools, they exhibit different activity levels. Girella laevifrons is highly
active and easy to detect in intertidal pools, while G. nigra is more cryptic and commonly found under rocks in caves (Fuentes, 1982; Shinen & Navarrete 2010; Flores &
Rendic, 2011). The two species studied also have different diets. Girella laevifrons are
omnivorous, consuming mainly macroalgae, bivalves, isopods and amphipods, all prey
items located in UV-exposed sectors of intertidal pools (Pulgar et al., 1999). Graus
nigra in contrast are carnivorous, mostly consuming decapods, amphipods, gastropods,
bivalves and polychaetes, prey which are located mainly in protected sectors (e.g. under
rocks) (Muñoz & Ojeda, 1997; Caceres & Ojeda, 2000; Fariña et al., 2000).
The aim of the study was to evaluate the effect of UV radiation on habitat selection
of G. laevifrons and G. nigra under laboratory conditions. Considering the different
habitat use exhibited by these two species, it was hypothesized that G. nigra will show
a significant change in the use of space when exposed to UV radiation compared with
G. laevifrons and that this physical variable will be a factor capable of modifying the
habitat selection in these intertidal vertebrates.
Juvenile individuals of Girella laevifrons [n = 21, mean ± s.e. standard length
(LS ) = 3⋅91 ± 0⋅45 cm] and Graus nigra (n = 15, mean ± s.e. LS = 4⋅89 ± 0⋅38 cm)
were captured at Quintay (33∘ 11′′ S; 71∘ 41′′ W), Chile. All animals were obtained
from upper intertidal pools using BZ-20 anaesthetic and were immediately deposited
into sea water with constant aeration and then transported to the laboratory (Lab. Eco
1, Andres Bello University, Santiago, Chile). In the same pools where the fish were
captured, a broadband radiometer was used to register the intensity of UV radiation
© 2014 The Fisheries Society of the British Isles, Journal of Fish Biology 2014, doi:10.1111/jfb.12566
U V R A D I AT I O N A N D I N T E RT I D A L F I S H E S
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over 12 h (between 0830 and 2000 hours) at 30 min intervals during days of both clear
and cloudy conditions. At the laboratory, all specimens were fed ad libitum for 15 days
in a recirculation system with filtered sea water at a controlled temperature between
17 and 18∘ C and salinity of 34. Water temperature in this setup was in agreement with
values registered by in the intertidal pools (Pulgar et al., 2005) and as no field data
exist for salinity, values according to data reported for marine habitats (Strub et al.,
1998) were used.
The experimental setup consisted of a 111 cm × 30 cm × 30 cm tank. The tank was
divided into three compartments with the same dimensions (c. 37 cm × 30 cm) by using
2 cm wide expanded polyethylene rectangles covered with aluminum foil. In order
to allow movement between the three sections, the expanded polyethylene rectangles
were placed 10 cm above the bottom of the tank, leaving enough space for the fishes
to circulate. To avoid light reflection between the sections, a thin dark plastic mesh
was used to cover the bottom of the tank. After the tank was prepared, 50 l of filtered
sea water were added to the tank. The first section of the tank had white light (WL)
provided by a fluorescent refrigeration tube (self-ballasted led tube lamp, UNINOV;
www.luxledchina.com). The second section was kept under no light (N/L) conditions,
and the third section was illuminated with ultraviolet light (UV). The UV light was
provided by a 40 W fluorescent tube (wavelength 350–400 nm, Phillips Actinic BL;
www.philips.com/lighting; and a Luminaria Tube (100Wsm wavelength 290–315 nm,
ZINGG ILUMINA; www.zingg.cl) that emits a constant concentration of 12 μw
cm−2 . In order to determine radiation levels in the experimental system, UV radiation
intensity over 10 trails was recorded for each section of the experimental system with
the lights on and off, providing data for a total of 60 trials. Field and experimental
UV quantifications were made using a radiometer (Sper Scientific UV Light Meter,
UVA/B, UV range 1–40 μw cm−2 , 280–400 nm wave length, ALBA AMBIENTE
LTDA; www.electronicaindustrial.cl) and all UV radiation measurements were made
at water level.
A total of 12 G. laevifrons and 10 G. nigra were used for the experiments on habitat
selection and a total of nine G. laevifrons and five G. nigra during control trials.
The number of fishes was a function of their natural abundances. The experimental
tests were developed as follows: once the experimental system had all of its lights
on, each fish was placed, one per trial, into the middle section of the experimental
tank (N/L) and left for 20 min, allowing them to fully explore the experimental
setup (Pulgar et al., 1999). Afterwards, a chronometer (Isport/OEM Model JG021;
http://isport.en.made-in-china.com) was used over a period of 30 min to quantify
the time that each fish spent in each section of the experimental tank (configuration
WL-N/L-UV). In order to avoid any bias in the responses from the placement of
the lights in the tank, the position of lights in the experimental system was changed
using the configuration UV-WL-N/L (G. laevifrons, n = 6). The total time spent
and number of times that each fish visited each one of the sections were measured.
The same individual was used for the determinations of times and number of visits,
and a different set of animals for control and for the experiments involving changes
in the position of the lights. For the control assays, all lights in the experimental
setup and laboratory were off, and the same experimental sequence was followed
and the same variables were quantified. After each experimental and control trial,
the water in the tank was replaced in order to keep the environmental conditions
constant.
© 2014 The Fisheries Society of the British Isles, Journal of Fish Biology 2014, doi:10.1111/jfb.12566
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UV radiation (mW cm–2)
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J . P U L G A R E T A L.
30
20
10
0
0
0900
1100 1300 1500
Time of day (hours)
1700
1900
Fig. 1. Ultra violet (UV) radiation levels measured in the central coast of Chile during days of clear ( ) and
cloudy ( ) conditions between 0800 and 1900 hours.
The time that both species of fish spent in each section of the experimental and control system was evaluated with repeated measures by ANOVA using general lineal
models (GLM), with normal distribution specified. The number of visits that the fishes
made to each of the three sections of the experimental system was analysed by contingency tables using chi-square test (STATISTICA v6.0, StatSoft; wwwstatsoft.com/)
(Zar, 1996).
The registered levels of UV radiation in the field during both clear and cloudy
conditions reached maximal values around 1300 hours: 32 and 11 mW cm−2 , respectively (Fig. 1). In the experimental system, the levels of UV radiation registered were
11⋅15 mW cm−2 in the UV section, 0⋅03 mW cm−2 in the WL section (this radiation
may represent a remnant of UV light) and 0⋅00 mW cm−2 in the N/L section. No radiation levels were registered for any section of the experimental system under control
conditions. During exposure to the experimental system, G. laevifrons and G. nigra
spent more time in the N/L section [G. laevifrons: two-way ANOVA, F 2, 22 = 9⋅01,
P = 0⋅001, G. nigra: two-way ANOVA, F 2, 12 = 8⋅25, P < 0⋅05; Fig. 2 (a), (b);
G. laevifrons: 95% c.i. = UV 251.60-696.14, WL 17.06-223.26, NL 585.16-1348.50.
G. nigra: UV 65.59-474.80, WL 75.94-611.05, N/L 721.28-1560.97]. The species
comparison indicated that G. laevifrons spent more time in the UV than WL section.
Graus nigra spent less time than G. laevifrons in the UV but similar in WL section
of experimental system (a posteriori Tukey test P ≤ 0⋅05, [Fig. 2 (a), (b) and Table I].
When the number of visits to the different sections of the experimental system was
evaluated, G. laevifrons visited the UV section more frequently, whereas G. nigra
showed an increased number of visits to the N/L and WL sections (𝜒 2 = 423⋅5,
d.f. = 2, P < 0⋅001; Fig. 3). In the experimental system with changes in the order of
the light sections (configuration UV-WL-N/L), the results for G. laevifrons indicated
a clear preference for the N/L section [two-way ANOVA, F 2, 10 = 141⋅08, P < 0⋅001;
Fig. 4 (a); 95% c.i. = UV 30.70-144.12, WL 82.78-218-52, N/L 842.39-1080.87]. No
differences in the number of visits to the different sections [Fig. 4 (b)] were observed,
supporting the previously indicated selectivity.
The control experiments showed that G. laevifrons and G. nigra spent similar
amounts of time and visited each one of the different tank sections with similar
frequency [time: G. laevifrons, two-way ANOVA, F 2, 16 = 1⋅94, P > 0⋅05 and G. nigra,
© 2014 The Fisheries Society of the British Isles, Journal of Fish Biology 2014, doi:10.1111/jfb.12566
5
U V R A D I AT I O N A N D I N T E RT I D A L F I S H E S
1·5
(a)
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1·0
Time of residency (s ×103)
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#
0·5
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*
(b)
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N/L
Treatment zones
WL
Fig. 2. Time that (a) Girella laevifrons ( ) and (b) Graus nigra ( ) spent in each experimental sector: ultraviolet
light (UV), white light (W/L) and no light sector (N/L). Values are mean + s.e. * P < 0⋅05 N/L v. UV and
WL for both species; # P < 0⋅05 G. laevifrons v. G. nigra.
F 2, 8 = 0⋅80, P > 0⋅05, Fig. 5 (a); visit: G. laevifrons, 𝜒 2 = 15⋅17, d.f. = 16, P > 0⋅05
and G. nigra, 𝜒 2 = 12⋅45, d.f. = 10, P > 0⋅05, Fig. 5 (b)].
The observations indicated that UV radiation in the experimental system was of intermediate magnitude compared with field evaluations (Fig. 1). It was also shown that UV
radiation affects space selection in the two species of intertidal fishes studied. Both
species showed a clear preference for the section with no light, and in agreement with
the present hypothesis, G. laevifrons visits the section with UV light more frequently
compared with G. nigra, evidence that may be associated to different habitat use by or
target species.
Several studies have shown that UV radiation generates ulcers and damages the skin,
eye structures and DNA in fishes (Bullock, 1982; Ahmed & Setlow, 1993; Cullen &
Monteith-McMaster, 1993; Cullen et al., 1994; Ramos et al., 1994; Vetter et al., 1999;
Lesser et al., 2001). Considering the negative effects of UV radiation, it is conceivable
Table I. General linear model analysis (ANOVA) comparing time that experimental groups of
Girella laevifrons and Graus nigra spent in each section of system
Effect
d.f.
MS
F
P
Time
Species
Experimental section
Species × experimental section
Error
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2
40
12 560⋅69
3418⋅48
7685⋅15
406⋅72
4⋅06
8⋅40
18⋅89
>0⋅05
<0⋅001
<0⋅001
© 2014 The Fisheries Society of the British Isles, Journal of Fish Biology 2014, doi:10.1111/jfb.12566
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Visits % of total
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40
20
0
UV
N/L
Treatment zones
WL
Fig. 3. Number of visits that Girella laevifrons ( ) and Graus nigra ( ) made to each experimental sector: ultraviolet light (UV), white light (W/L) and no light sector (N/L). Total number of visits recorded = 2054.
that this exposure also alters patterns of spatial occupancy of intertidal fishes. This
may be especially relevant for species that inhabit an environment highly affected by
UV radiation, such as the upper intertidal zone. Recently, a high antioxidant capability
was reported for G. laevifrons exposed to experimental UV radiation (Carrasco-Malio
et al., 2014).
The observation that both G. laevifrons and G. nigra actively selected the N/L section
in the experimental setup (Fig. 2), suggests that mobile and cryptic intertidal fishes are
able to modify their activity patterns in response to light. This evidence also suggests
that in the field, fishes exposed to different light types would be capable of relating
these habitat traits to the potential risks associated with UV light, e.g. exposure to biotic
and abiotic risks (Zagarese & Williamson, 2001; Häder et al., 2003; Nava et al., 2011).
(a)
Time of residency (s ×103)
1·5
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J . P U L G A R E T A L.
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UV
WL
Treatment zones
NL
Fig. 4. (a) Time spent and (b) number of visits made by Girella laevifrons in each experimental sector: ultraviolet
light (UV), white light (W/L) and no light sector (N/L). Total number of visits recorded = 369. Values are
mean + s.e.
© 2014 The Fisheries Society of the British Isles, Journal of Fish Biology 2014, doi:10.1111/jfb.12566
U V R A D I AT I O N A N D I N T E RT I D A L F I S H E S
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Visits % of total
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UV
N/L
Treatment zones
WL
Fig. 5. (a) Time spent and (b) number of visits made by Girella laevifrons ( ) and Graus nigra ( ) in each
experimental sector in control conditions: ultraviolet light (UV), white light (W/L) and no light sector (N/L).
Total number of visits recorded per species: G. laevifrons = 1051 and G. nigra = 562. Values are mean + s.e.
The present results also showed that G. laevifrons visited the UV section more frequently and spent more time there [Figs 2 (a) and 3] compared with G. nigra. As
G. laevifrons is the more active of the two species evaluated and G. nigra are mostly
found under rocks or in intertidal pool crevices (Fuentes, 1982; Flores & Rendic, 2011),
it is conceivable that this differential response is associated to a greater UV tolerance
in G. laevifrons (Carrasco-Malio et al., 2014) than G. nigra. Moreover, the behaviour
of G. laevifrons suggests the ability to differentiate zones in a tidal pool where it is possible to find food, such as where algae and invertebrates reside (Metaxas & Scheibling,
1994).
It has been suggested that the amount of UV radiation could be a factor that generates differential behavioural responses in intertidal fishes (Leech et al., 2009; Ingolf &
Bakker, 2010), with a more intense predatory response in highly mobile animals. The
results are in agreement with reported evidence indicating that marine animals employ
two common strategies to avoid UV damage: staying away from UV exposure (e.g. to
live under rocks, in caves, in an opaque shell or at great depth) or acquiring (by synthesis or sequestration) a UV-absorbing ‘sunscreen’ (Zamzow, 2004; Lars, 2007). The
results also suggest a different tendency in space use in response to UV exposure in
intertidal fishes.
In summary, the observations highlight the presence of two strategies used by
intertidal fishes to avoid UV damage; to spend more time hidden under crevices as
observed for G. nigra and G. laevifrons, or to show increased UV tolerance as observed
for G. laevifrons. The latter appears to be positively correlated with the levels of UV
radiation to which this mobile species is normally exposed to in intertidal pools. As
UV exposure modifies space use by highly mobile predators, such as intertidal fishes,
the extended effects on the intertidal community (e.g. those due to changes in their
foraging), need to be addressed.
© 2014 The Fisheries Society of the British Isles, Journal of Fish Biology 2014, doi:10.1111/jfb.12566
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This study was funded by grants DI 17-10R, DI 16-12/R and DI-495-14/R Universidad Andres
Bello awarded to JP, internal grants Universidad Central de Chile to MA and DI-02-11/I Universidad Andres Bello MRG-H. This work was developed during tenure of Littoral Ecology Course
2012, Universidad Andres Bello. The authors are grateful to A. Jeffers for language revision of
the article.
References
Ahmed, F. E. & Setlow, R. B. (1993). Ultraviolet radiation-induced DNA damage and its photorepair in the skin of the platy- fish Xiphophorus. Cancer Research 53, 2249–2255.
Bothwell, M. L., Sherbot, D. M. J. & Pollock, C. M. (1994). Ecosystem response to solar
ultraviolet-B radiation – Influence of trophic level interactions. Science 265, 97–100.
Bridges, C. R. (1994). Ecophysiology of intertidal fish. In Fish Ecophysiology (Rankin, J. C. &
Jensen, F. B., eds), pp. 375–399. London: Chapman & Hall.
Bullock, A. M. (1982). The pathological effects of ultraviolet radiation on the epidermis of
teleost fish with reference to the solar radiation effect in higher animals. Proceedings of
the Royal Society of Edinburgh B 81, 199–210.
Caceres, C. W. & Ojeda, F. P. (2000). Foraging patterns of two species of intertidal herbivorous
fishes: effect of food abundance and chemical composition. Revista Chilena de Historia
Natural 73, 253–260.
Carrasco-Malio, A., Días, M., Mallea, M., Montoya, M. J., Miranda, A., Landaneta, M. F.,
Sánchez, G. & Hidalgo, M. E. (2014). Are the intertidal Fish highly resistant to Uv-B
radiation? A study based on oxidative stress in Girella laevifrons (Kyphosidae). Ecotoxicology and Environmental Safety 100, 93–98. 10.1016/j.ecoenv.2013.07.030.
Cullen, A. P. & Monteith-McMaster, C. A. (1993). Damage to the rainbow trout (Oncorhynchus
mykiss) lens following an acute dose of UVB. Current Eye Research 12, 97–106.
Cullen, A. P., Monteith-McMaster, C. A. & Sivak, J. G. (1994). Lenticular changes in rainbow
trout following chronic exposure to UV radiation. Current Eye Research 13, 731–737.
Dayton, P. K. (1971). Competition, disturbance and community organization: the provision and
subsequent utilization of space in a rocky intertidal community. Ecological Monographs
41, 351–389.
Fariña, J. M., Aldana, M., Ogalde, F. & Ojeda, F. P. (2000). Trophic ecology of Girella laevifrons
(Pisces: Kyphosidae) in rocky intertidal zones of northern Chile affected and non-affected
by copper mine tailings. Revista Chilena de Historia Natural 73, 139–149.
Flores, H. & Rendic, J. (2011). Conducta alimenticia, supervivencia y crecimiento de juveniles
silvestres de Graus nigra Philippi, 1887 en cautiverio (Perciformes: Kyphosidae). Latin
American Journal of Aquatic Research 39, 607–612.
Fuentes, H. R. (1982). Feeding habitats of Graus nigra (Labridae) in coastal waters of Iquique
in Northern Chile. The Japanese Journal of Ichthyology 29, 95–98.
Gosselin, L. A. & Chia, F. S. (1995). Distribution and dispersal of early juvenile snails: effectiveness of intertidal microhabitats as refuges and food sources. Marine Ecology: Progress
Series 128, 213–223.
Häder, D. P., Kumar, H. D. & Smith, R. C. (2003). Aquatic ecosystems: effects of solar ultraviolet radiation and interactions with other climatic change factors. Photochemical Photobiological Science 2, 39–50.
Häder, D. P., Helbling, E. W., Williamson, C. E. & Worrest, R. C. (2011). Effects of UV radiation
on aquatic ecosystems and interactions with climate change. Photochemical Photobiological Science 10, 242–260.
Helbling, E. W., Villafañe, V., Ferrario, M. & Holm-Hansen, O. (1992). Impact of natural ultraviolet radiation on rates of photosynthesis and on specific marine phytoplankton species.
Marine Ecology: Progress Series 80, 89–100.
Hofmann, L. C., Yildiz, G., Hanelt, D. & Bischof, K. (2012). Physiological responses of the
calcifying rhodophyte, Corallina officinalis (L.), to future CO2 levels. Marine Biology
159, 783–792.
Hughes, L. (2000). Biological consequences of global warming: is the signal already apparent?
Trends in Ecology & Evolution 15, 56–61.
© 2014 The Fisheries Society of the British Isles, Journal of Fish Biology 2014, doi:10.1111/jfb.12566
U V R A D I AT I O N A N D I N T E RT I D A L F I S H E S
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
9
Ingolf, P. R. & Bakker, T. C. M. (2010). Ultraviolet light influences habitat preferences in a fish
under predation risk. Evolutionary Ecology 24, 25–37.
Jokiel, P. L. & York, R. H. Jr. (1984). Importance of ultraviolet radiation in photo inhibition of
microalgal growth. Limnology and Oceanography 29, 192–199.
Kiffney, P. M., Clements, W. H. & Cady, T. A. (1997). Influence of ultraviolet radiation on the
colonization dynamics of a Rocky Mountain stream benthic community. Journal of the
North American Benthological Society 16, 520–530.
Lamb, E. A., Leslie, H. M. & Shinen, J. S. (2014). Both like it hot? Influence of temperature
on two co-occurring intertidal barnacles in central Chile. The Journal of Experimental
Biology 453, 54–61.
Lars, O. (2007). Photobiology. The Science of Life and Light, 2nd edn. New York, NY:
Springer-Verlag.
Leech, D. M., Padeletti, A. & Williamson, C. E. (2009). Zooplankton behavioral responses
to solar UV radiation vary within and among lakes. Journal of Plankton Research 27,
461–471.
Lesser, M. P., Farrell, J. H. & Walker, C. W. (2001). Oxidative stress, DNA damage and
p53 expression in the larvae of Atlantic cod (Gadus morhua) exposed to ultraviolet
(290–400 nm) radiation. The Journal of Experimental Biology 204, 157–164.
Little, C. & Kitching, J. A. (1996). The Biology of Rocky Shores. Oxford: Oxford University
Press.
McNamara, A. E. & Hill, W. R. (1999). Effects of UV-B dose and irradiance: comparison
between grazers. Journal of the North American Benthological Society 18, 370–380.
Metaxas, A. & Scheibling, R. E. (1993). Community structure and organization of tide pools.
Marine Ecology: Progress Series 98, 187–198.
Metaxas, A. & Scheibling, R. E. (1994). Spatial and temporal variability of tidepool hyperbenthos on a rocky shore in Nova Scotia, Canada. Marine Ecology: Progress Series 108,
175–184.
Muñoz, A. A. & Ojeda F. P. (1997). Feeding guild structure of a rocky intertidal fish assemblage
in central Chile. Environmental Biology of Fishes 49, 471–479.
Nava, S., Stephen, A. & Hamil, T. (2011). Visual detection of UV cues by adult zebra fish (Danio
rerio). Journal of Vision 11, 1–5.
Navarrete, S. A., Gelcich, S. & Castilla, J. C. (2012). Long-term monitoring of coastal ecosystems at Las Cruces, Chile: defining baselines to build ecological literacy in a world of
change. Revista Chilena de Historia Natural 83, 143–157.
Paine, R. S. (1977). Controlled manipulations in the marine intertidal zone, and their contribution to ecological theory. Special Publications of the Academy of Natural Science
Philadelphia 12, 245–270.
Pulgar, J. M., Bozinovic, F. & Ojeda, F. P. (1999). Behavioral thermoregulation in the intertidal
fish Girella laevifrons (Khyphosidae): the effect of starvation. Marine and Freshwater
Behaviour and Physiology 32, 27–38.
Pulgar, J. M., Bozinovic, F. & Ojeda, F. P. (2005). Local distribution and thermal ecology of two
intertidal fishes. Oecologia 142, 511–520.
Pulgar, J. M., Ojeda, F. P. & Bozinovic, F. (2006). Intraspecific geographic and seasonal physiological variability in an intertidal fish along a climate gradient. Journal of Fish Biology
68, 1–7.
Pulgar, J. M., Bozinovic, F. & Ojeda, F. P. (2007). Inter-population thermal variability and physiological response in the intertidal fish Scartichthys viridis (Blenniidae). Revista Chilena
de Historia Natural 80, 439–446.
Pulgar, J., Poblete, E., Alvarez, M., Morales, J. P., Aranda, B., Aldana, M. & Pulgar, V. M.
(2013). Can upwelling signals be detected in intertidal fishes of different trophic levels?
Journal of Fish Biology 83, 1407–1415.
Ramos, K. T., Fries, L. T., Berkhouse, C. S. & Fries, J. N. (1994). Apparent sunburn of juveniles
paddlefish. Progressive Fish-Culturist 56, 214–216.
Shinen, J. L. & Navarrete, S. A. (2010). Coexistence and intertidal zonation of chthamalid barnacles along central Chile: interference competition or a lottery for space? Journal of
Experimental Marine Biology and Ecology 392, 176–187.
Sousa, W. P. (1979). Experimental investigation of disturbance and ecological succession in a
rocky intertidal algal community. Ecological Monographs 49, 227–254.
© 2014 The Fisheries Society of the British Isles, Journal of Fish Biology 2014, doi:10.1111/jfb.12566
10
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
J . P U L G A R E T A L.
Strub, P. T., Mesias, J. M., Montecinos, V., Rutllant, J. & Salinas, S. (1998). Coastal ocean
circulation off western South America coastal segment (6, E). In The Sea (Robinson, A.
R. & Brink, K. H., eds), pp. 273–308. New York, NY: John Wiley & Sons.
Tadetti, M. & Sempéré, R. (2006). Penetration of ultraviolet radiation in the marine environment.
A review. Photochemical Photobiological Science 82, 389–397.
Vetter, R. D., Kurtzman, A. L. & Mori, T. (1999). Diel cycles of DNA damage and repair in eggs
and larvae of Northern anchovy, Engraulis mordax, exposed to solar ultraviolet radiation.
Photochemical Photobiological Science 69, 27–33.
Wahl, M., Molis, M., Davis, A., Dobretsov, S., Durr, S. T., Johanssons, J., Kinley, J., Kirugara,
D., Langer, M., Lotze, H., Thiel, M., Thomason, J. C., Worm, B. & Ben-Yosef, D. (2004).
UV effects that come and go: a global comparisons of marine benthic community levels
impact. Global Change Biology 19, 1962–1972.
Watkins, E. M., Schindler, D. W., Turner, M. A. & Findlay, D. (2001). Effects of solar
ultraviolet radiation on epilithic metabolism, and nutrient and community composition
in a clear-water boreal lake. Canadian Journal of Fisheries and Aquatic Sciences 58,
2059–2070.
Zagarese, H. & Williamson, C. E. (2001). The implications of solar UV radiation exposure for
fish and fisheries. Fish and Fisheries 2, 250–260.
Zamzow, J. P. (2003). Ultraviolet-absorving compounds in the mucus of temperate Pacific tide
pool sculpins: variation over local and geographic scales. Marine Ecology: Progress
Series 263, 169–175.
Zamzow, J. P. (2004). Effects of diet, ultraviolet exposure, and gender on the ultraviolet
absorbance of fish mucus and ocular structures. Marine Biology 144, 1057–1064.
Zar, J. H. (1996). Biostatistical Analysis, 3rd edn. Englewood Cliffs, NJ: Prentice-Hall Inc.
© 2014 The Fisheries Society of the British Isles, Journal of Fish Biology 2014, doi:10.1111/jfb.12566