Ecological Indicators 46 (2014) 232–239
Contents lists available at ScienceDirect
Ecological Indicators
jo ur nal ho me page: www.elsevier.com/locate/ ecolind
Physiological and biochemical thermal stress response of the
intertidal rock goby Gobius paganellus
Diana Madeira
a,∗
, Vanessa Mendonc ¸ a
b
, Marta Dias
b
, Joana Roma
b
, Pedro M. Costa
c
,
Mário S. Diniz
a
, Catarina Vinagre
b
a
REQUIMTE, Departamento de Química, Centro de Química Fina e Biotecnologia, Faculdade de Ciências e Tecnologia, Universidade Nova de Lisboa,
2829-516 Caparica, Portugal
b
Centro de Oceanografia, Faculdade de Ciências, Universidade de Lisboa, Campo Grande, 1749-016 Lisboa, Portugal
c
IMAR – Instituto do Mar, Departamento de Ciências e Engenharia do Ambiente, Faculdade de Ciências e Tecnologia, Universidade Nova de Lisboa,
2829-516 Caparica, Portugal
a r t i c l e i n f o
Article history:
Received 26 January 2014
Received in revised form 5 May 2014
Accepted 23 June 2014
Keywords:
Gobius paganellus
Climate change
Critical thermal maximum
Hsp70
Ubiquitin
a b s t r a c t
The intertidal habitat is characterized by environmental conditions with steep gradients. Thus, inhabiting
communities have long served as models in stress research. Moreover, several studies have reported
their vulnerability to climate change and consequent distribution shifts (up to 50 km per decade) and
abundance changes. The aims of this study were to test the effects of temperature on the rock goby
Gobius paganellus in order to understand its resistance to environmental fluctuations (e.g. low tide events,
heat waves) and gain insights into its vulnerability to climate change. The upper thermal limit for the
species was estimated through the critical thermal maximum (CTMax). Individuals were exposed to a
temperature increase ramp of 1
◦
C h
-1
. Two thermal stress biomarkers (hsp70 and total ubiquitin) were
quantified in the gill, muscle and liver via enzyme linked immunosorbent assays. Results showed no
increases in hsp70 in neither of the organs in response to temperature but ubiquitin levels were elevated
in liver at 30
◦
C. Both biomarker basal levels were higher in gills, followed by liver and finally muscle. The
results indicate that the species, although adapted to the intertidal environment, can experience stress at
high temperatures of 30
◦
C and above. Therefore, it may be vulnerable to heat waves, especially occurring
during low tides that coincide with the hottest hours of the day during summer, with adverse implications
in a climate change scenario that predicts temperature rising and increasing (in length and frequency)
periods of extreme heat. The present study also shows that different organs possess distinct heat stress
thresholds and responses, hence the importance of multi-organ approaches in order to comprehend the
full health status of the organisms following acute thermal challenge.
© 2014 Elsevier Ltd. All rights reserved.
1. Introduction
The intertidal habitat is characterized by environmental con-
ditions with steep gradients (Menge and Branch, 2001; Tomanek
and Helmuth, 2002; Hofmann, 2005) that can become harsh to its
inhabiting communities. These habitats are in between the terres-
trial and marine realms, imposing the conditions of aquatic and
aerial regimes on its living organisms (Helmuth et al., 2006). Several
environmental factors are of extreme importance in these habi-
tats, such as solar radiation, wind, wave exposure and temperature
∗
Corresponding author. Tel.: +351 21 2948500; fax: +351 212948554.
E-mail address: dianamadeira@netcabo.pt (D. Madeira).
among others (Bell, 1995; Helmuth, 1999; Stenseth et al., 2003).
Temperature is of general importance as it affects marine life at sev-
eral levels (Hochachka and Somero, 2002). It determines metabolic
rates and reactions, behavioral responses (Mora and Ospina, 2001)
and severely affects the performance of ectotherms (Porter and
Gates, 1969). Additionally, it influences the organisms’ growth
(e.g. Phillips, 2005), feeding (e.g. Sanford, 2002), reproduction (e.g.
Philippart et al., 2003) and ultimately survival (Dallas and Rivers-
Moore, 2012). Finally, temperature sets ecological patterns at the
population and ecosystem level (Walther et al., 2002; Gaston, 2003;
Helmuth et al., 2006). Considering this, intertidal organisms are
subjected to environmental challenges and must possess certain
adaptations in order to successfully colonize those habitats. Thus,
these organisms have been widely used in stress research and may
http://dx.doi.org/10.1016/j.ecolind.2014.06.029
1470-160X/© 2014 Elsevier Ltd. All rights reserved.