Behavioural responses of talitrid amphipods to ...

Journal of Experimental Marine Biology and Ecology 486 (2017) 170–177

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Behavioural responses of talitrid amphipods to recreational pressures on oceanic tropical beaches with contrasting extension Filipa Bessa a,⁎, Felicita Scapini b, Tatiana M.B. Cabrini c,d, Ricardo S. Cardoso c a

MARE – Marine and Environmental Sciences Centre, Faculdade de Ciências e Tecnologia, Universidade de Coimbra, 3004-517 Coimbra, Portugal Dipartimento di Biologia, Università degli Studi di Firenze, Via Romana, 17, 50125 Florence, Italy Laboratório de Ecologia Marinha, Departamento de Ecologia e Recursos Marinhos, Universidade Federal do Estado do Rio de Janeiro (UNIRIO), Rio de Janeiro, RJ, Brazil d Programa de Pós-graduação em Ecologia, Universidade Federal do Rio de Janeiro, Brazil b c

a r t i c l e

i n f o

Article history: Received 24 June 2016 Received in revised form 6 October 2016 Accepted 8 October 2016 Available online xxxx Keywords: Sandy beaches Urbanisation Recreation Atlantorchestoidea brasiliensis Orientation Bioindicator

a b s t r a c t Ocean sandy beaches are prime sites for human recreation. The integrity of these ecosystems may suffer greatly from tourism-related pressures. Behavioural adaptations of fauna are key traits as responses to environmental pressures and short time changes. In particular, orientation performance of talitrid amphipods to recover the optimal zone on the beach has been proposed as bioindicator of shoreline stability, mainly related to sedimentary dynamics and geomorphological changes. The question focused here was whether recreational activities and urbanisation may influence orientation performance of talitrids on oceanic tropical beaches with contrasting extension (beach length). Field orientation experiments were performed during Spring 2014 testing populations of the talitrid Atlantorchestoidea brasiliensis on four tropical beaches at Rio de Janeiro (Brazil), selected according to their human access (two with and two without public access) and length (two pocket and two extended beaches). The influence of landscape cues on the orientation of talitrids was experimentally tested in two etho-assay conditions: with and without the landscape vision. Talitrids used landscape cues and sun compass to orient seawards and the highest precision of orientation was recorded in the pocket beach without human access. A more scattered response was observed in the urbanised pocket beach under conditions of screened landscape and when the sun was veiled or covered by clouds, showing the importance of the local landscape features in these conditions. The populations from the extended beaches showed a similar and more scattered orientation, which may be interpreted as behavioural plasticity to cope with beach natural changes, disregarding human pressure on the beaches. The behavioural performances of talitrids on the four tropical beaches varied according to different human pressure conditions and beach extension, confirming the reliability of the use of talitrid orientation as bioindicator of beach changeability. © 2016 Elsevier B.V. All rights reserved.

1. Introduction Sandy beaches are the most extended ecological interface systems between land and sea and are characterised by variable morphological and ecological conditions, resulting in highly dynamic habitats (McLachlan and Brown, 2006). The society greatly values these naturally occurring assets, which, when left intact, may support both ecological processes and sustainable use (McLachlan and Brown, 2006; Schlacher et al., 2007, 2015). Coastal urbanisation and recreational activities may create direct pressures on beach ecosystems, which may compromise their ecological integrity and in consequence economic value and even public appeal (Brown and McLachlan, 2002; Defeo et al., 2009; Harris et al., 2015). ⁎ Corresponding author. E-mail address: [email protected] (F. Bessa).

http://dx.doi.org/10.1016/j.jembe.2016.10.007 0022-0981/© 2016 Elsevier B.V. All rights reserved.

The general paradigm of beach ecology holds that beaches are resilient to human uses and recognizes that resident fauna have specific adaptations to inhabit this dynamic environment (McLachlan and Brown, 2006). Beach macrofauna have developed key behavioural adaptations in order to successfully establish on sandy beaches such as mobility, burrowing ability, rhythmicity and orientation, characterised by plasticity to face natural changes (Defeo and Gomez, 2005; Scapini, 2006, 2014). Intensive human use of beaches has been recognised to negatively affect beach fauna and specific impacts of recreational activities are well documented, such as pedestrian trampling (Weslawski et al., 2000; Veloso et al., 2006, 2008; Ugolini et al., 2008; Schlacher and Thompson, 2012; Bessa et al., 2013a, 2014) and damages caused by off-road vehicles (Schlacher et al., 2008), as well as disturbances to behaviour profiles of birds (Schlacher et al., 2013). In this regard, macroinvertebrates have been considered good bioindicators of beach ecological condition, including their taxonomic diversity and

F. Bessa et al. / Journal of Experimental Marine Biology and Ecology 486 (2017) 170–177

abundance, range of physiological tolerance to stress, behavioural plasticity and life-history strategies (e.g. Scapini and Ottaviano, 2010; Veloso et al., 2008; Bessa et al., 2013a, 2013b, 2014; Nourisson et al., 2014; Schlacher et al., 2014; Scapini et al., 2015). These traits allow macrofauna to respond to a wide range of potential beach modifications, including possible coastline retreat due to climate global change. One particular well-studied trait is the orientation behaviour expressed by talitrid amphipods, key species in temperate and tropical sandy beaches, which are able to return to the optimal beach zone (zonal orientation) from a distant point, not directly linked with the goal, using the sun compass and additional cues, e.g., landscape vision, beach slope and wind (reviewed in Scapini, 2006, 2014 and references therein). The sun compass is genetically fixed in populations where the shoreline has not changed in time (long term, allowing several generations, Scapini et al., 1985), while on highly dynamic (eroded, accreting or changing orientation) shorelines talitrids tend to scatter or orient using local landscape features (Ugolini et al., 1986; Scapini et al., 1995). A learning capacity, based on a calibration of sun compass to local landscape cues was observed in populations of the talitrid Talitrus saltator from dynamic beaches (Ugolini and Macchi, 1988; Scapini, 2006). There are a considerable number of studies that demonstrate that sandhoppers calibrate the sun compass by adjusting their orientation with respect to local cues, when naturally or accidentally displaced from their optimal zone on the beach (e.g., Fanini et al., 2007; Bessa et al., 2013a, 2013b; Scapini et al., 2015). Accordingly, the orientation of talitrids may represent an immediate response to environmental changes and play a major role in ecosystem resilience under disturbance conditions (Scapini, 2014). This capability have been considered a good estimator of beach perturbations, namely those related with sedimentary modifications, such as the construction of seawalls, beach nourishment and artificial dunes (Fanini et al., 2007, 2009; Scapini et al., 2005; Nourisson et al., 2014; Bessa et al., 2014). Scapini et al. (2015) proposed the sun orientation of talitrid amphipods as a bioindicator of beach stability in terms of shoreline changes due to modified or interrupted sedimentary transport, as observed in extended versus pocket beaches. The concept of beach stability involves a complex combination of interactions of geologic, oceanographic, meteorological and, to a lesser extent, biological processes and may occur across a broad range of spatial and temporal scales (McLachlan and Brown, 2006). High levels of urbanisation and human activities may also influence beach stability altering their profiles, sedimentary dynamics and consequently may affect beach fauna, but the effects of these impacts are difficult to discern from naturally occurring changes of such dynamic environments (Defeo et al., 2009; McLachlan et al., 2013) and need to be estimated. Beach ecologists have considered beach length as an important element on beach morphodynamics and surf-zone circulation having consequences for local macrofauna populations (Brazeiro, 1999; McLachlan and Brown, 2006; Cardoso et al., 2012). However, much of the scientific knowledge on beach ecology concerns exposed extended beaches and there is still significant scope for gaining further insights into the way the morphodynamics of smaller (pocket) beaches may influence beach communities and their capacity to withstand potential environmental changes, either natural or human-induced (Deidun and Schembri, 2008; Cardoso et al., 2012; Scapini et al., 2015). Most work on pocked beaches was done in the Mediterranean Basin, where tide and swash regimen are limited in extension, experiments on oceanic tropical beaches were interesting to verify the hypothesis illustrated above of the dependence of macrofauna behavioural adaptations on beach morphodynamics. The talitrid Atlantorchestoidea brasiliensis (Dana, 1853) is one of the most important species structuring the macrofaunal assemblages of exposed sandy beaches of Rio de Janeiro in Brazil (Cardoso and Veloso, 1996, 2001; Cardoso, 2002). Still there was no information regarding their behavioural adaptations, namely orientation strategies to maintain/recover the optimal zone on the beach when displaced under

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different environmental conditions. A sizeable body of literature has evidenced the intensive human use and habitat changes that occurs on beaches from Rio de Janeiro (e.g. Veloso et al., 2006, 2008; Cardoso et al., 2016) offering the opportunity to test the behavioural skills of the talitrid Atlantorchestoidea brasiliensis for the first time on oceanic tropical beaches. The goal of this study was to provide an assessment of the behavioural adaptations of the talitrid amphipod Atlantorchestoidea brasiliensis on tropical beaches, and to analyse the effects of recreational human use and urbanisation of beaches, as well as beach extension on the orientation performances of this species. In particular, the question was open to whether the orientation with landscape cues (high buildings backing the beach) would allow orientation seawards under covered sky. The hypotheses tested were: 1) urbanisation and recreational activities negatively affect talitrid orientation behaviour; 2) populations on pocket beaches show better adapted (more precise seawards) orientation than populations on extended exposed beaches, likely subject to changing sedimentary transport; 3) populations on urbanised beaches use human constructions as landscape cues.

2. Materials and methods 2.1. Study sites and urbanisation level Four tropical ocean beaches located along 60 km of the coast of Rio de Janeiro (Brazil) were selected to test the behavioural adaptation (i.e. orientation performance) of the talitrid Atlantorchestoidea brasiliensis (Fig. 1). Beaches were selected according to their extension: two pocket beaches b 1000 m in length, limited by natural headlands (representing each a cell for sediment transportation and currents) and two extended beaches with a length of several kilometres, exposed to dominant winds and currents. Additionally, these beaches were selected taking into account their recreational uses: i.e. two with free public access and highly urbanised beaches (sensu Veloso et al., 2006) versus two protected beaches where human access is limited (Fig. 1). For this purpose, the extended (13 km) beach Restinga da Marambaia (23°03′S, 43°30′W) was selected (Fig. 1). This beach has fine sand and is classified as very exposed (according to the classification of McLachlan, 1980), of intermediate morphodynamics type and with a wide surf zone (Caetano et al., 2006; Cardoso et al., 2016). Restinga da Marambaia beach is located in a Brazilian Military area where public human access is not permitted. To assess the effect of beach extension a similarly protected beach with fine sand was selected, but with lower extension (500 m) - the pocket beach Fora (22°57′ S, 43°11′W), which is a reflective beach nested in between rocky headlands and is also located in a military area with restricted public visitation (Veloso and Cardoso, 1999). Additionally, two urbanised beaches with contrasting extension were selected: the extended beach “Barra da Tijuca” and the pocket beach “Prainha” (Fig. 1). Barra da Tijuca (35°15′S, 11°2′W) is an exposed beach 16.5 km long (Fig. 1). The most urbanised section was selected which measures about 8 km (Alvorada) and is interrupted by a protected sector (about 4 km, Reserva), with the remaining 4.5 km also urbanised. This area has free access for public, crowded neighbourhoods and many recreational amenities (restaurants, bars, hotels and boardwalks among others), which provide the ideal conditions for the access of visitors all year-round. In terms of morphodynamics, Barra da Tijuca is an intermediate beach with medium grain size (Veloso et al., 2008). The secluded 800 m long Prainha beach (23°25′S, 43°25′W), which is one of the best-known surfing beaches in Rio de Janeiro; for this reason it is highly frequented all year-round. Cardoso and Veloso (1996) characterised this pocket beach as reflective and exposed with medium sand. Detailed information regarding the sediment properties and classification of beaches (Beach Index and exposure) are available in Cardoso et al. (2016).

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D C

A B

Atlantic Ocean

Fig. 1. Location of study sites selected on the Rio de Janeiro coast (south-eastern Brazil), comprising two beaches where human access is permitted (grey symbols) and two without free human access (black symbols) and with contrasting extensions (pocket beaches – smaller symbols; extended beaches – bigger symbols). A – Restinga da Marambaia, B – Prainha, C – Barra da Tijuca and D – Fora.

The level of urbanisation of each beach was estimated using a modified version of the Urbanisation Index developed by González et al. (2014) taking into account 6 (the Urbanisation Index uses 7) indicators/variables: proximity to urban centres, buildings on the sand, beach cleaning, solid waste in the sand, vehicle traffic on the sand and frequency of visitors. The quality of night sky, which is also included in the index, was not assessed (the sky quality was not relevant to this study, which was carried out during the day to test sun orientation) and therefore it was not included in the calculation. Each indicator/variable was estimated for each beach according to the levels of human intervention (low, medium and high) following González et al. (2014) rationale (see the Supplementary material). The level of proximity to the city and the presence of buildings, solid waste on the sand and the intensity of vehicle traffic were estimated by direct observation on the beach and information from previously published articles from the authors (e.g. Cardoso et al., 2016). For the frequency of visitors, a proxy was used by recording the number of visitors on each beach during the experimental days, with zero counts recorded in the military protected beaches (Fora and Restinga da Marambaia, Table 1). The resulted Urbanisation indicator value ranges from 0 to 1; where values close to “0” indicate beaches with low human pressures and values close to “1” indicate beaches with high human pressure (for more details regarding the calculations of the Urbanisation Index please consult González et al., 2014 and the Supplementary material).

2.2. Orientation experiments Orientation tests on the talitrid Atlantorchestoidea brasiliensis were carried out during spring 2014 (November and December) on the four selected beaches. At each experimental session a profile of the beach was determined from the waterline to the base of the dunes (when present) using standard topographic methodologies; other beach features (dimensions, slope, shoreline direction) were also recorded. To perform the orientation experiments, sensu etho-assay (Scapini et al., 2015), a transparent, Plexiglas arena with 40 cm diameter and 72 pitfall traps of 5° each at its rim was placed on the supralittoral zone of the beach on a small horizontal table at one meter above the sand surface, so that the experimental observers could not be seen by the talitrids released in the arena. The pitfall trap 72 was oriented to the North (full details of the protocol are available in Scapini et al., 2005). Adult talitrid amphipods were collected by hand from the sand in the morning of the experiments during low tide and tested in a series of eight releases of ten individuals in the morning (9:00–10:00 a.m., solar time) and eight in the afternoon (3:00–4:00 p.m., solar time), using each time different individuals. An opaque white cylindrical screen covered the arena around the transparent Plexiglas screen at alternate releases, to have one release with the landscape vision allowed and the following one with only the visibility of the sun permitted.

Table 1 Beach features and population traits recorded during the orientation experiments in each beach. TED: Theoretical Escape Direction seawards, N: number of individuals tested. Pocket beaches

Beach length (m) Beach width range (m) Seaward direction -TED (°) Mean beach slope (1/m) ± SD Mean grain size (mm)a Mean air temperature ± SD (°C) Mean air humidity ± SD (%) Cloudiness (0/8) N Sex ratio (M:F) Mean cephalic length (mm) ± SD Antenna articles (mm) ± SD a

From Cardoso et al. (2016).

Extended beaches

Fora (protected)

Prainha (urbanised)

Restinga (protected)

Barra (urbanised)

430 24–26 100 11.89 ± 0.96 0.35 37.72 ± 3.78 42.91 ± 20.46 0–1 300 0.49 0.81 ± 0.12 15.05 ± 1.8

800 36–38 180 14.17 ± 5.79 0.44 40.79 ± 7.45 41.73 ± 12.82 0–1 305 0.69 0.74 ± 0.13 13.93 ± 1.94

13,000 42–60 210 20.61 ± 6.64 0.26 37.61 ± 6.83 47.75 ± 17.71 1–6 300 0.63 0.81 ± 0.11 15.07 ± 1.69

17,000 46–48 200 7.19 ± 4.12 0.51 32.49 ± 5.49 47.90 ± 8.36 0–4 331 1.11 0.87 ± 0.11 15.43 ± 1.70


During each release the following variables were registered: time of the day (h), air humidity (%, electronic thermo-hygrometer), air temperature (°C, electronic thermo-hygrometer), sun vision (visible, veiled, shape, not visible; visual appreciation) and sky cloudiness (0–8 scale, visual appreciation). The wind was not considered as the Plexiglas arena does screen it off. The random variables above may influence orientation performance under natural conditions. Therefore a suitable number of replicates were made. In principle, each individual performance may be considered a replicate; the ten individuals released at the same time had the same external conditions, but could have differed for the intrinsic variables (size, age and sex). The directional choice of the individuals within each group was assumed to be independent, as talitrids do not influence each other when orienting in the test arena (after Scapini et al., 1981). The angle of escape (degrees from North) was recorded for each individual via the trap number and all specimens tested were stored in alcohol 75% for later measurement in the laboratory of intrinsic variables, namely the cephalic length and the number of segments of the second antennae as proxies of size and age, respectively (Marques et al., 2003). The sex of each individual tested was also observed later in the laboratory and registered. Each individual was sexed using the stereomicroscope and sorted into: (a) males, with a developed second gnathopod; (b) females, with oostegites and without a developed second gnathopod; (c) juveniles, lacking both oostegites and a developed second gnathopod (Cardoso and Veloso, 1996). The sun azimuth was estimated from the geographic coordinates of the site, the date and time of the day of each release. On each test day, the density of beach visitors was estimated for an area of 50 m2 as a proxy of beach human use. The number of persons was counted every 15 min (between 09:00 and 15:00 h) during the orientation experiments.

2.3. Circular data analyses The distributions of orientation angles of talitrids were analysed using the statistics of circular distributions (Fisher, 1993) within SPlus Insightful software, using a library developed ad hoc (Marchetti and Scapini, 2003). For each angle distribution the circular plot was drawn and the following statistics were calculated: the mean angle (with 95% confidence intervals), the mean vector length (r) and the Rayleigh test for uniformity, to assess the null hypothesis of random orientation. The probability density curves, smoothed with the kernel method, were estimated and double plotted on Cartesian graphs to visualise the peaks of the circular distributions (Fisher, 1993). Kuiper's test for two samples comparison adapted to large samples was performed to estimate if circular distributions differed significantly for mean direction, angular variance or any property (i.e. circular dispersion and vector length; Batschelet, 1981). Multiple regression analyses adapted to circular data (SPLM, Spherically Projected Linear Models; Marchetti and Scapini, 2003) were applied to verify the significance of the variables and factors recorded during the tests to the variation of orientation angles. The environmental conditions recorded during each release and the individual information on the talitrids tested in each experiment (October and November) were included separately as replicates. This analysis allowed us to compare the angular distributions observed under (varying) natural conditions, taking into account the random factors that might have influenced orientation, other than the factors under test: pocket vs. extended beach; urbanised vs. protected beach; visible landscape vs. landscape screened off. All the variables and factors taken into account were included in the baseline model, which was then compared with other models with a lower number of parameters. The best model was evaluated having the highest likelihood with the minimum number of parameters, using the Akaike Information Criterion (AIC). The significance of each factor was estimated by

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means of the Likelihood Ratio Test (LRT) on the difference between the best model and the model without the specific factor under test. 3. Results 3.1. Beach environment, human use and urbanisation level Beach meteorological conditions during the experimental sessions were similar on the four beaches, with minimal monthly differences in air temperature, humidity and sun visibility (Table 1). The sites differed mainly in their physical dimensions and human use, with the two pocket beaches (Fora and Prainha) ranging between 430 m and 800 m in beach length while the two extended beaches (Restinga da Marambaia and Barra da Tijuca) ranged from 13,000 to 17,000 m (Table 1). The lowest values of the Urbanisation Index belonged to the protected beaches Restinga da Marambaia and Fora (0.07 and 0.17, respectively, Table 2) where the access to visitors was limited. In contrast, the highest urbanisation levels occurred at Prainha and Barra da Tijuca (0.47 and 0.73, respectively), which are touristic beaches with free public access (the number of visitors ranged from 50 to 80 individuals on 50 m2 during each experimental session, Table 2) located in the urban area of the city of Rio de Janeiro. 3.2. Orientation performance of talitrid populations The population structure of the talitrids Atlantorchestoidea brasiliensis recorded during the experimental sessions showed similar mean cephalic lengths (proxy of size) and similar number of antennae articles (proxy of age) of the individuals on all beaches analysed (Table 1). The sex ratio was considerably female biased except for the urbanised extended beach Barra da Tijuca that was male biased (Table 1). The effect of landscape vision on orientation was revealed by the significant differences observed in each population when tested with and without landscape vision (Kuiper's test on normalised angles, p b 0.001, Fig. 2 and Table 3). A more concentrated seawards orientation was observed in all beaches when the landscape vision was allowed, with the mean circular distribution values (orientation mean angle ± confidence interval) including the Theoretical Escape Direction – TED (Table 3, Fig. 2). All populations had unimodal angular distributions, shown by the density-estimated curves and were significantly different from random distribution (Rayleigh's tests for uniformity p b 0.001, Table 3). However, in the condition of visible landscape, a better orientation (Kuiper's test, p b 0.001) was shown on the pocket beaches of Fora and Prainha, where the circular dispersion was lower, mean resultant vector length higher and confidence interval narrower (Table 3). Further comparisons were performed to investigate the effect of human access to the beaches on talitrid orientation when the landscape was visible and no significant differences were observed on both pocket

Table 2 Urbanisation Index (González et al., 2014) calculated for each beach based on the quantification of urbanisation indicators (0 corresponds to the total absence and 5 to an extremely high level of urbanisation). The number of visitors (n/50 m2) recorded during the experimental sessions is presented in brackets. Additional information about the indicators is available in the supplementary material.

Proximity to downtown Buildings on the sand Cleaning of the beach Solid waste in the sand Vehicle traffic Demand by visitors (n/50 m2) Urbanisation Index

Pocket beaches

Extended beaches

Fora

Prainha

Restinga

Barra

2 1 2 0 0 0 (0) 0.17

1 3 3 3 0 5 (50) 0.47

0 0 0 2 0 0 0.07

4 4 4 3 2 5 (80) 0.73

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Fig. 2. Distribution plots of Atlantorchestoidea brasiliensis orientation tested on sandy beaches with contrasting human access and extension in two distinct test conditions, with and without the visibility of the landscape. White arrows represent the TED (Theoretical Escape Direction seawards) and the small black triangles the individual directions. The kernel density estimates are double plotted in the Cartesian graphs on the right to show all peaks in the 360°. The summary statistics of the distributions are presented in Table 4.

and extended beaches with respect to beach access (Kuiper's test, p N 0.05). The etho-assays testing the influence of landscape visibility (screen/ no screen) revealed in general a higher scatter of the talitrids tested with the screen, with significant differences between pocket and extended beaches (Kuiper's test, p b 0.001, Fig. 2). However, the recreation and urbanisation pressures only influenced the orientation of the populations from the pocket beaches (Kuiper's test p b 0.001, Fig. 2). Talitrids

from the protected beach of Fora were still North-east oriented when neither sun nor landscape were visible, and in this beach the circular distributions showed the best precision in orientation compared to all other beaches (r = 0.55 and Sample Circular Dispersion = 0.96), while the highest scatter was recorded on the urbanised pocket beach of Prainha with two peaks of angles shown by the kernel graph (r = 0.45 and Sample Circular Dispersion = 1.87, Fig. 2 and Table 3). Regarding the extended beaches, a similar scatter was obtained for both

Table 3 Summary statistics of the orientation angular distributions of talitrids shown in Fig. 2.

Pocket

Beach

Test condition

Mean direction (°)

Confidence interval 95% (°)

Mean vector length (r)

Circular dispersion

N

Fora

Landscape view No landscape view Landscape view No landscape view Landscape view No landscape view Landscape view No landscape view

98.35 115.40 178.70 176.90 213.90 211.10 206.00 172.60

±5.28 ±10.39 ±5.10 ±11.60 ±5.97 ±10.89 ±6.28 ±10.90

0.86 0.55 0.84 0.45 0.80 0.52 0.77 0.46

0.22 0.96 0.22 1.87 0.41 1.76 0.37 1.77

159 141 152 153 159 141 168 163

Prainha Extended

Restinga Barra

For all orientation tests Rayleigh test: p b 0.001.


beaches disregarding the human access to the beaches (Kuiper's test, p N 0.05), with similar values of mean vector lengths and dispersion in the distribution angles (Table 3). SPLM analysis of orientation showed a significant interaction between the “beach” factor and all the other variables and factors in the best model (compared to the baseline additive model through the AIC) and consequently four models were developed for each beach (Table 4). Each beach best model retained three factors: the time of day, a meteorological variable (air humidity or temperature) and landscape visibility, which highlights the influence of other cues than sun compass in the orientation of the populations tested. The main differences in the beach best models were observed among beaches with contrasting extension: the extended beaches retained the environmental variables (air temperature and air humidity) in their models, while the pocket beaches retained mainly the variables related with visual cues, such as the “landscape vision” and the “sky cover” (Table 4). 4. Discussion Behavioural studies using talitrid amphipods as models were mainly performed on temperate Mediterranean and Atlantic beaches (e.g. Fanini et al., 2007; Fanini et al., 2009; Scapini et al., 2005, 2015; Bessa et al., 2013a, 2013b; Nourisson et al., 2014), where the differences observed in sun orientation performance of talitrids represented a clear indication of beach disturbances, particularly related with changes in sedimentary dynamics, e.g. accretion versus erosion and artificially stabilized beaches versus natural dynamics. In the present study, a similar approach was employed testing for the first time the behavioural performance of talitrids on Atlantic tropical beaches as response indicator to anthropogenic habitat disturbances, particularly those related with beach recreation and urbanisation pressures (compare the indices of Table 2). It is well known that most popular coastal areas like those belonging to the urban area of Rio de Janeiro are susceptible to present fragile ecosystems that suffer greatly from tourism-related impacts (Cardoso et al., 2016). Actually, the beaches that recorded high urbanisation values (Prainha and Barra da Tijuca) were touristic beaches, where human interventions were noticeable, including the presence of access facilities and artificial lighting on the beach, which contributed to the increase in visitors number all day and night and consequently may increase the pressures on beach macrofauna. To this regard, biological and ecological effects of human activities are well documented in the most urbanised beaches of Rio de Janeiro, where significant declines in abundances of talitrids were reported (Veloso et al., 2006, 2008; Cardoso et al., 2016). In this study, was tested how human pressures may affect the behavioural adaptations of the species Atlantorchestoidea brasiliensis and if anthropogenic pressures act differently on beaches with contrasting extension (pocket versus extended beaches). Most research on the effects of trampling on invertebrate fauna concerned the survival of the population (e.g. Weslawski et al., 2000; Ugolini et al., 2008; Veloso et al., 2008), but the potential stress to the

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navigational capacity of talitrids due to human trampling was not yet accessed. The use of sun compass by talitrids to recover the optimal zone on the beach is well recognised, and the use of landscape features to help orientation is well demonstrated (reviewed in Scapini, 2006). Talitrids, when naturally or accidentally displaced on the beach, tend to return to the optimal beach zone, the driftline, by using the sun compass and landscape cues to orient seawards. However, when punctual disturbances like those from recreational activities (e.g., human trampling, sediment movement and transport) occur, the orientation mechanisms can be affected. Talitrids have high behavioural plasticity and remarkable ability to learn new directions on the beach when pressure disturbance occurs (Scapini, 2006). The results of the orientation tests of this study carried out on Brazilian beaches revealed that talitrids had high precision in their orientation in all beaches selected, when they were able to see the landscape. Nevertheless, significant differences were observed between beaches when the landscape vision was screened off and the sun was the only orientation cue. In these conditions, talitrids may have encountered difficulties to orient appropriately to the seaward direction, in particular in the highly urbanised pocket beach, where a high dispersion of individuals was observed. In contrast, in the pocket beach with limited human access (Fora) talitrids showed the best performance with clear seawards orientation even without access to landscape cues. The orientation seawards that was observed on Fora beach when both the sun and landscape were covered may depend on other visual cues, such as differences in intensity, colour or polarisation of sky light (Scapini, 2006), in fact, the sky was not completely covered during the experiments (6/8 cloudiness). Ad hoc experiments should be made on tropical Brazilian beaches to clarify this point. These results revealed that a precise mechanism such as the sun compass in conjunction with lower disturbance on beaches where human access was restricted (Fora) favoured a higher precision in orientation. These results are in accordance with the conceptual model proposed by Scapini (2014), which considers that the behaviour of talitrids might be expressed at different levels of flexibility/rigidity, according to beach changeability/stability. Despite the concept of beach stability in beach ecology is complex and often refers to changes in sedimentary conditions (McLachlan and Brown, 2006), here unstable beach environments are associated with disturbances related to intense human use of beaches (such as pedestrian trampling) and physical changes caused by activities linked with urbanisation on coastal areas (e.g., parking areas and construction of beach facilities), which in turn may alter the space available on the beach for the resident fauna and also contribute to changes in sedimentary features and dynamics (Schlacher and Thompson, 2012, for tropical beaches in Australia). A similar behavioural field experiment performed on beaches along the Uruguayan coastline on the talitrid Atlantorchestoidea brasiliensis examined the influence of beach morphodynamics on orientation (Fanini et al., 2009). The stability conditions in the supralittoral zone of a reflective beach favoured a higher precision of sun orientation of talitrids, where the supralittoral zone was more protected from the wave energy and the environment was more stable than on a dissipative beach (Fanini et al., 2009).

Table 4 Baseline and best additive multiple regression models and best model containing the interaction with “beach” (SPLM) for the total dataset and the best model for each beach selected through the Akaike Information Criterion (AIC). Likelihood Ratio Test for the single factors: *p b 0.05; **p b 0.01; ***p b 0.001. Model

Score

Baseline model Orientation ~ beach + month + time of the day + sun azimuth + landscape vision + air temperature + air humidity + sky cover + sun visibility + number of persons + sex + size + age Best additive Orientation ~ beach*** + landscape vision*** + time of the day*** + sun azimuth*** + sun visibility*** + air humidity*** + model month** + sky cover** Best model Orientation ~ beach*(landscape vision*** + sun azimuth*** + sky cover*** + air temperature* + month* + age*) Barra Orientation ~ landscape vision*** + time of the day*** + air humidity Restinga Orientation ~ landscape vision*** + time of the day*** + air temperature** Fora Orientation ~ sky cover*** + time of the day*** + landscape vision*** Prainha Orientation ~ landscape vision*** + time of the day*** + sky cover**

AIC 3121.66 df 1236 AIC 3112.45 df 1250 AIC 2789.80 df 1216 AIC 831.19 df 323 AIC 679.16 df 290 AIC 507.89 df 288 AIC 507.41 df 258

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Fig. 3. Conceptual model of orientation performances of Atlantorchestoidea brasiliensis on oceanic tropical beaches with contrasting extension and human access.

In the present study carried out on the same species in tropical beaches, the orientation performance was enhanced by the landscape vision, as pointed out by the significance of the factor “landscape vision” in the models obtained with the SPLM analysis. In addition, on the two protected beaches, the best behavioural adaptation of talitrids in both conditions (with and without landscape vision) was observed in the pocket beach without public access (Fora). This result is in agreement with the theoretical model of orientation of talitrids proposed by Fanini et al. (2009), which suggested that higher environmental stability would enhance a higher precision in sun orientation and consequent no need of integration with other visual cues such as the landscape. Thus, variation in the orientation performance of talitrids responded to the higher stability observed on a smaller scale in our study: the pocket beach with limited human interference. Additionally, these results are in line with the findings of Scapini et al. (2015) performed on Mediterranean coasts, where on pocket beaches the sun orientation of talitrids was more precise than on extended ones. In that study there was no difference in the degree of urbanisation between the selected beaches, being all highly urbanised (Scapini et al., 2015). In our case, populations from both the extended beaches (with and without the human pressure) had similar performances of orientation, with a higher scatter in orientation when the landscape was screened off. These populations revealed in general a smaller precision in orientation performance and high influence of the climatic conditions when compared with the populations from the pocket beaches. This was confirmed by the presence in the best models of the variables related to the dehydration risk of talitrids, namely air temperature and humidity, which are consistent with the higher risk offered on beaches where the distances to the optimal zone are wider (in Brazil, beach width and length were higher on the two extended beaches). Scapini et al. (2015) found that the extension of the beach negatively affected orientation of talitrids on the Mediterranean coasts and discussed that extended beaches may be more subject to longshore sediment transport due to the higher exposition to winds and currents than pocket beaches, a pattern also recorded in this study. In sum, our results strongly support the hypothesis that behavioural responses of talitrids are influenced by a range of possible interacting factors, which may result also from recreational activities, urbanisation and natural physical variability of beaches. Nevertheless, seasonal variations in environmental conditions may also influence the orientation mechanisms of talitrids, as recorded in temperate environments (e.g. Nourisson and Scapini, 2014), and thus time scale to assess variation in the behaviour should also consider seasonality even if fluctuations in tropical regions are less evident regarding temperature changes and more related to disturbances due to rainfalls or storms. The behavioural responses of talitrids translated into the precision of orientation seawards through the statistics of angular distributions is best expressed by the length of the mean vector (r, a measure of dispersion around the mean) and has been proposed as a potential bioindicator for the impact of sedimentary dynamics on sandy beaches

(Scapini et al., 2015). Here, this notion is reinforced by adding to this concept that human recreation and urbanisation may also affect the behavioural adaptation of talitrids in particular in pocket beaches were the human effect was significant (Fig. 3). An open question was: which variable (extension or human use) affected more the orientation? At the end it cannot be ensured which variable was more important to define orientation performances of talitrids. On one hand, they performed better on pocket beaches, but the recreation/urbanisation effects were higher again on pocket beaches. On the extended beaches in turn, a more flexible orientation of talitrid was observed disregarding the human access. For those reasons a combination of both factors was significant (as resulted from the multiple regression analysis), also highlighting that human access had influence mainly on pocket beaches (Fig. 3). It is important to highlight that the experimental settings under natural environmental conditions, the impossibility of a complete control of morphodynamic and environmental features (for example the dissipative character and the gentle slope of the beach Restinga da Marambaia make it clearly distinguishable from the other beaches), the relative contribution on each individual variable/stressor and the linkages with the life-history traits of amphipods (Gómez et al., 2013) might affect the outcome of the etho-assays and should be taken in consideration for future conceptual designs for beach experiments. Nevertheless, the interpretation of the behavioural responses in the light of intensive recreational pressures on pocket sandy beaches recorded in this study provides evidence of potential negative ecological effects that might occur in highly urbanised coasts. Finally, the behaviour of talitrids, representing a rapid response to environmental changes, may have a major role in permitting the survival of these populations in the beach environment and may be used in an interdisciplinary approach as an assessment tool of beach condition.

Acknowledgments This study was supported by FAPERJ (Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro, E26/111.182/2014). This study has also the support of Fundação para a Ciência e Tecnologia (FCT) through the strategic project UID/MAR/04292/2013, granted to MARE. Filipa Bessa furthermore acknowledges the financial support received from the FCT through her post-doc scholarship (SFRH/BPD/99747/ 2014). Tatiana M.B. Cabrini was supported by CNPq (Brazilian National Council for Scientific and Technological Development) and by Universidade Federal do Rio de Janeiro (UFRJ) Ricardo S. Cardoso was supported by FAPERJ and CNPq. We also thank the team from ECOMAR for assistance during the experimental sessions. [SS] Appendix A. Supplementary data Supplementary data to this article can be found online at http://dx. doi.org/10.1016/j.jembe.2016.10.007.


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