Marine Pollution Bulletin xxx (2014) xxx–xxx
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Effect of coastal urbanization on sandy beach coleoptera Phaleria maculata (Kulzer, 1959) in northern Chile Sergio A. González ⇑, Katherine Yáñez-Navea, Mauricio Muñoz Departamento de Biología Marina, Facultad de Ciencias del Mar, Universidad Católica del Norte, Casilla 117, Coquimbo, Chile
a r t i c l e
i n f o
Keywords: Marine tenebrionid Phaleria maculata Anthropogenic impact Coastal urbanization index Light pollution
a b s t r a c t The beetle Phaleria maculata is a common inhabitant of the upper intertidal fringe of Chilean beaches. Anthropogenic intervention in coastal areas has increased intensely, leading to changes in the flora and fauna of sandy beaches. To examine the impact of human activities on P. maculata, we studied several beaches along the northern Chilean coast. Beaches were characterized based on morphodynamics and the level of intervention, leading to the estimation of an ‘‘Urbanization Index’’ based on various indicators. The analysis showed a significant inverse correlation between the rate of urbanization and night sky quality. Larval and adult beetles were almost absent on beaches with high levels of urbanization. The results of simple and multiple correlations based on nMDS ordination showed an inverse relationship between increases in urbanization and the abundance of beetles. Because darkling beetles are very sensitive to human interventions on sandy beaches, we suggest that they are ideal indicator organisms for the health of these environments. Ó 2014 Elsevier Ltd. All rights reserved.
1. Introduction The growing human pressure on natural systems results in strong impacts, some of which may be irreversible. Halpern et al. (2008) noted that at present, all marine ecosystems have been affected by human activities, especially in the coastal zone. In the case of Latin America, a classification based on an estimate of a Threat Index has shown that the coasts of Brazil, Peru and Ecuador are subject to the greatest impacts (Chatwin and Rybock, 2007). The major threats to biodiversity in South America are fisheries, pollution, urbanization, mining, the oil industry, aquaculture, shipping, invasive species, and climate change. Among these threats, the urbanization of the coastal zone in parts of Latin America has been very rapid, following the regional economic boom and leading to ‘‘sun and beach tourism’’. The high demand for seaside spaces, lack of institutional experience with handling this demand and the limitations of scientific knowledge on the dynamics of coastal ecosystems and the impacts on natural systems have been identified as major factors causing deterioration of coastal environments (Dayton, 2003; Orams, 2003; Dias et al., 2012). In general,
⇑ Corresponding author. Address: Departamento de Biología Marina, Facultad de Ciencias del Mar, Universidad Católica del Norte (UCN), Larrondo 1281, Casilla 117, Coquimbo, Chile. Tel.: +56 51 2209786; fax: +56 51 2209812. E-mail address: [email protected] (S.A. González).
coastal ecosystems are very sensitive to the impacts associated with mass tourism (Dadon, 2002). As more and more beaches are urbanized, natural resources become more valuable not only for permanent residents but also for tourists looking for pristine beaches and clear waters, clean air and natural sounds, among other features (Roca and Villares, 2008; Roca et al., 2009). In recent decades, human impacts on sandy beaches have strongly increased, resulting in a significant alteration of their flora and fauna (Brown and McLachlan, 2002; Schlacher et al., 2007, 2008; Defeo et al., 2009). Globally, many of the sandy beaches close to urban areas have undergone complete removal of landward dunes due to construction of roads and buildings (Morteiro and Bemvenuti, 2006), dramatically transforming these environments. The pursuit of economic growth through the exploitation of recreation and tourism on beaches has generated intensive urban growth, resulting in major disruptions to natural communities by intense trampling of fragile sandy beach habitats during the summer (Comor et al., 2008), the incorporation of solid waste (Thiel et al., 2003; Bravo et al., 2009), and the passage of vehicles (Gheskiere et al., 2006; Veloso et al., 2008). Moreover, the intense use of sandy beaches as recreational sites and the growing demand for ‘‘quality’’ by the users have forced local authorities in many countries to mechanically remove flotsam (natural and anthropogenic) from beaches, further altering the natural habitat (Ryan and Swanepoel, 1996; Defeo et al., 2009; MacLachlan et al., 2013). Human activities in many highly touristic
http://dx.doi.org/10.1016/j.marpolbul.2014.03.042 0025-326X/Ó 2014 Elsevier Ltd. All rights reserved.
Please cite this article in press as: González, S.A., et al. Effect of coastal urbanization on sandy beach coleoptera Phaleria maculata (Kulzer, 1959) in northern Chile. Mar. Pollut. Bull. (2014), http://dx.doi.org/10.1016/j.marpolbul.2014.03.042
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S.A. González et al. / Marine Pollution Bulletin xxx (2014) xxx–xxx
areas require lighting, resulting in dense coverage of artificial lights along these beaches, which not only affects the natural habitats but also leads to a gradual ‘‘disappearance’’ of starlight (Smith, 2009). Consequently, many coastal habitats, communities and ecosystems are exposed year-round to the impact of artificial light (Longcore and Rich, 2004; Navara and Nelson, 2007; Hölker et al., 2010). This relationship between artificial night lighting and human development has been an indicator of levels of urbanization in the fields of economics and remote-sensing engineering (Ghosh et al., 2010; Ma et al., 2012; Zhang and Seto, 2013), but it has received little attention from marine ecologists. Although little studied, tenebrionid beetles are common organisms on sandy beaches, being described as ‘‘sensitive’’ to environmental perturbations (Veloso et al., 2008; Comor et al., 2008). These organisms are dominant in the upper part of the beach, presenting morphological and ecophysiological adaptations that confer resistance to lack of freshwater and to high temperatures (Colombini et al., 1994). Due to the high biomass of local beetle populations (larvae and adults) on sandy beaches, they play a key ecological role in coastal environments, facilitating the processes of fragmentation and decomposition of plant and animal remains, as well as the activation of nutrient cycles, particularly in those ecosystems where microbial action is restricted due to low humidity (Santos et al., 1988; Cepeda-Pizarro, 1989; Cartagena et al., 2002). These beetles also play an important ecological role as mobilizers of matter and energy between the marine and terrestrial ecosystems (Cheng, 1976). On the Pacific coast of South America, adults and larval stages of Phaleria maculata (Kulzer, 1959) (formerly Phalerisida maculata) can be commonly found under kelp debris and other organic matter stranded in the supralittoral fringe of the beach (Peña, 1996; Vidal and Guerrero, 2007). In Chile, there have been various studies of sandy beaches (Hernández et al., 1998; Contreras and Jaramillo, 2003), but the ecological role of these organisms is poorly known (Avellanal et al., 2000; Jaramillo et al., 2003, 2006). Like other countries in Latin America, the Chilean government is making efforts to promote tourism (Barragán, 2001; Santana, 2003). Various coastal administrations in north-central Chile have based their economic development on tourism, which has involved a greater degree of building both recreational and residential structures in close proximity to the beaches. This increasing urbanization may affect the fauna of the beach, but this has not yet been evaluated. For this reason, the present study assesses the level and effect of various factors related to urbanization on the abundance of the marine darkling beetle P. maculata along a stretch of coast in the Region of Coquimbo, in northern Chile. We test the hypothesis that intensive coastal development causes a decrease in the abundance of these beetles.
2. Methods 2.1. Study area Twelve sandy beach locations were sampled along 100 km of the Coquimbo seashore in northern Chile (Fig. 1). The sampling sites show different degrees of urbanization. Some beaches, La Herradura, Changa, northern Tongoy and Peñuelas, are integrated into the city, where they are in high tourist demand and close to paved roads that include night lighting, kiosks selling food, residential buildings and high-rise buildings. In summer, there is a clear increase in the amount of solid waste in the sand because of the high presence of visitors, such that municipal administrators rake the beach with heavy machinery. Other beaches, such as Caleta Hornos, Morrillos, Las Mostazas and southern Tongoy, are far from
urban centers, where the level of intervention is low compared to urban beaches.
2.2. Physical characterization The beach slope of each location was estimated from the height difference between the drift line and water line (Emery, 1961). To estimate the morphodynamic state of the beach, the Dean parameter (X) (Wright and Short, 1984) was used; three samples of sediment were collected at the drift line, separated by approximately 50 m, using a core of 4 cm in diameter which was buried up to 15 cm. Particle size and average grain size were determined using a settling tube. The sedimentation rate of the particles was evaluated based on tables from Gibbs et al. (1971) on the basis of the calculation of average particle size using the ‘‘computational method of moments’’ (Seward-Thompson and Hails, 1973). The wave height was estimated using a centimeter ruler and aligned with the horizon, for 10 waves on each of three occasions separated by approximately 30–45 min. The period of the wave, considered as the elapsed time (seconds) between two waves that break, was measured on three occasions separated by 30–45 min, using a digital stopwatch to count the waves that occurred in 5 min.
2.3. Urbanization level The level of urbanization was estimated by calculating an index with 7 variables: (1) Proximity to urban centers, (2) Building on the sand, (3) Beach cleaning, (4) Solid waste on the sand, (5) Vehicle traffic on the sand, (6) Quality of the night sky, and (7) Frequency of visitors. These indicators were systematized through a rubric featuring low, medium, and high ‘‘levels of development’’ (Table 1). In turn, each level was divided into two scores (0–1, 2–3 and 4–5) to give greater certainty to the estimate, ‘‘0’’ could be indicated in the case of the complete absence of the variable estimated, versus ‘‘5’’ when extremely high levels were observed. The level of proximity to the city and the presence of buildings, solid waste on the sand and traces of vehicle traffic were estimated by direct observation in the field. The night sky quality was assessed using magnitude charts for the nighttime sky from the NOAO ‘‘Globe at Night’’ Program as reference (www.globeatnight.org). For beach cleaning and frequency of visitors, in addition to field observations, information provided by the National Tourism Service (SERNATUR Chile) and Municipal Administrators was considered. Urbanization index was calculated using the method of Gover, X0 = ((X–Xmin)/(Xmax–Xmin)) (Legendre and Legendre, 1998), which reduced the indicator values to a range [0–1]; where X is the value assigned to each of the seven variables and Xmin–Xmax corresponds to the extreme values of the range (0–5 in this case). Index values ranking close to ‘‘0’’ indicating beaches with low human intervention and sectors with values close to ‘‘1’’ indicating beaches with high human intervention. Additionally, to evaluate the relationship between this index and the night lighting, the night sky quality was determined using SQM-L (Sky Quality Meter). For this case, 5 measurements were taken at each point at different angles of orientation toward the sky. The SQM-L allows objective measurements of the quality of the sky, incorporating a highly sensitive photometer that measures the brightness of the sky (only visible light) at a particular angle of the sky. The data were expressed on a logarithmic scale of magnitudes per square arcsecond (MPSAS), which ranges from a value of 17 for highly polluted skies and 23 for dark skies (visit http://unihedron.com for more details). To reduce variations, the measurements were made over a period of two consecutive days with clear skies and at 23:00 h.
Please cite this article in press as: González, S.A., et al. Effect of coastal urbanization on sandy beach coleoptera Phaleria maculata (Kulzer, 1959) in northern Chile. Mar. Pollut. Bull. (2014), http://dx.doi.org/10.1016/j.marpolbul.2014.03.042
S.A. González et al. / Marine Pollution Bulletin xxx (2014) xxx–xxx
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Fig. 1. Locations of 12 studied beaches in the IV Región de Coquimbo, northern Chilean coast. CHN = North and CHS = South side of Caleta Hornos; CSP = Caleta San Pedro; P = Caleta Peñuelas; PCH = Playa Changa; LHN = North and LHS = South side of Bahía La Herradura; PM = Playa Morrillos; LM = Playa Las Mostazas, and TN = North, TC = Center and TS = South side of Bahía Tongoy.
2.4. Abundance of P. maculata Although the zonation of sandy beach macroinfauna has been described for Chile (Jaramillo, 1987), a systematic and intensive beach-level sampling design was used (James and Fairweather, 1996) where the beetle population is concentrated (Jaramillo et al., 1993; Jaramillo et al., 2006). At each study site, the abundance of P. maculata larvae and adults was recorded at 3 sampling stations separated by 50 m. At each sampling station, 10 transects were established perpendicular to the coastline and separated by 1.5 m. Each transect had 3 levels, one higher than 1.5 m above the drift line, a medium level exactly on the drift line, and a low level located 1.5 m below the drift line. This involved a total of 30 samples per station and 90 samples in total per sector. Larvae and adults of P. maculata were collected with a core of 0.1 m that was buried 20 cm in the sand. The sample was sifted using 1-mm mesh and then carried to the water to remove sand and thereby collect fauna, which were fixed with a solution of 70% alcohol in seawater. Samples were analyzed in the laboratory for the quantification of larvae and adults. 2.5. Analysis Possible differences in the abundance of P. maculata (larvae, adults and total) between the beaches sampled were studied using non-parametric analysis of k independent samples with the Kruskal–Wallis test (H, P = 0.05) because not all of the assumptions required by parametric tests were met. The same statistical analysis was used to assess the significance of differences in morphometric characteristics and the quality of night sky between the beaches studied. An a posteriori Tukey test was used to discriminate between the beaches studied when differences were significant. The correlation between the mean abundance of P. maculata (larvae, adults and total) and the characteristics of the sampled sites (geomorphological characteristics, urbanization index, and night sky quality) were evaluated by Spearman non-parametric
correlation analysis, and the significance was evaluated based the critical value of ‘‘r’’ at a level of 0.05 (Zar, 1999) using SPSS 17. To provide an integrative approach and only for comparative purposes, the abundance of P. maculata (adults, larvae and total) was plotted on the MDS ordination – 2D sampling sites based on human intervention variables used to estimate the ‘‘urbanization index’’. This ordination was made using a Euclidean distance matrix using transformed data (log x + 1) and subsequently grouped using the UPGMA technique, in the statistical program Past. Subsequently, to obtain a measure of this relationship, the values of the first two dimensions of the MDS plot that grouped the sampling sites were compared with the P. maculata mean abundance using a multiple regression analysis. The significance of the value of r2 was assessed by ANOVA (F, P < 0.05) (Zar, 1999). 3. Results 3.1. Beach characteristics 3.1.1. Morphodynamics The sampled areas showed varying characteristics, from beaches that had an approximate width of 26 m in Caleta San Pedro to the case of south Caleta Hornos, which featured a beach of approximately 63 m wide. Similarly, the beach slope ranged from 1°, as with Playa Peñuelas, up to more than 5°, as in Las Mostazas. The mean recorded values for grain size corresponded to medium sand, with the exception of south Caleta Hornos, Caleta San Pedro, Peñuelas and north La Herradura, which showed fine sand. Of the morphodynamic states of the sampled sites, Caleta Hornos and Caleta San Pedro beaches are intermediate in character (1 < X < 6), with a moderate energy. However, the south Caleta Hornos showed increased wave height compared with the other areas of study. The beaches Peñuelas, Changa, La Herradura, Morrillos, Las Mostazas and Tongoy were classified as reflective beaches (X < 1), with low energy. However, in this category, Playa Changa and Bahía La Herradura, both northern and southern sectors, presented the lowest values of the Dean’s parameter (Table 2). Only
Please cite this article in press as: González, S.A., et al. Effect of coastal urbanization on sandy beach coleoptera Phaleria maculata (Kulzer, 1959) in northern Chile. Mar. Pollut. Bull. (2014), http://dx.doi.org/10.1016/j.marpolbul.2014.03.042
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S.A. González et al. / Marine Pollution Bulletin xxx (2014) xxx–xxx
Table 1 Qualitative indicators of human intervention used in estimating the level of beach urbanization in northern Chile. Beach urbanization indicator levels Low 0–1
Medium 2–3
High 4–5
Proximity to urban centers Buildings on the sand
Sector with rural character. Several kilometers away from urban center. No direct influence of an urban center on the beach No nearby buildings appreciable
Sector located c. 1 km from an urban center, showing some effects on the beach, such as noise, some lighting and nearby vehicles passing
Sector just meters from an urban center, the city virtually integrated. The beach is next to vehicular traffic, with evident noise and urban lighting
There are buildings close to the beach but not on the sand or the dunes
There are buildings that occupy the space at the beach or in the dunes
Cleaning of the beach
The beach is not ‘‘cleaned’’ by mechanical means, with no sand removal
Although mechanically engaged for cleaning, this is done infrequently, no more than 1 time per week. No frequent removal of sand
Beach is repeatedly cleaned by mechanical means, more than once a week, which causes frequent removal of the sand
Solid waste in the sand
No waste in the sand or the amount of waste on the beach is minimal
In a short walk of a few meters, some solid waste can be seen on the sand, such as paper, plastic containers and cigarette butts
Clearly a high frequency of solid waste on the sand, including papers, plastic containers, cigarette butts, plastic debris, scrap wood and glass
Vehicles traffic on the sand
No vehicle tracks were observed on the sand. There is no vehicle access on the beach
Although there are traces of vehicle passage, they are scarce. Vehicular crossing is not periodic and not constant. Vehicular access to the beach is relatively limited
There are many tracks, showing recurring vehicular traffic. Various vehicles have access to the beach
Quality of the night sky
Sky conditions are optimal for stargazing. The sky appears black, and hundreds of stars can be seen perfectly
The glow of artificial light moderately impaired conditions for stargazing. The sky appears dark gray, and some tens of stars can be seen with some difficulty
Given the high brightness of the artificial lighting, the conditions for stargazing are bad. The sky is gray and occasional stars can be seen. Light pollution is evident
Frequency of visitors
The area is visited by very few people, and those are located in areas isolated from each other. Rural beach
The sector has a moderate demand for use. Although it has tourists, based on either location or privacy, it does not have a large number of users
Sector in high demand from users, considered a high tourist beach. Public access urban beach
Table 2 Characterization of the study sites in terms of sand grain size, beach morphodynamics and night sky quality. Beach sampling locations
Mean grain size (mm) ðX_ SDÞ
Dean’s parameter (X)
Night sky quality (MPSAS) ðX_ SDÞ
North Caleta Hornos South Caleta Hornos Caleta San Pedro Peñuelas Playa Changa North La Herradura South La Herradura Morrillos Las Mostazas North Tongoy Central Tongoy South Tongoy
0.34 ± 0.030 0.18 ± 0.028 0.25 ± 0.034 0.20 ± 0.021 0.37 ± 0.022 0.22 ± 0.031 0.31 ± 0.048 0.35 ± 0.015 0.37 ± 0.020 0.31 ± 0.003 0.35 ± 0.026 0.29 ± 0.004
3.49 5.26 2.19 0.46 0.10 0.09 0.07 0.75 0.63 0.32 0.20 0.40
21.10 ± 0.35 21.04 ± 0.34 19.67 ± 0.55 18.08 ± 1.30 17.52 ± 1.65 17.30 ± 1.46 18.82 ± 0.51 20.20 ± 0.25 21.04 ± 0.22 20.57 ± 0.57 21.11 ± 0.37 21.37 ± 0.14
X showed significant differences among sampling sites (H = 61.930, P = 0.00); the other variables did not differ among the beaches. 3.1.2. Night sky quality The areas of north and south La Herradura, Playa Changa and Peñuelas showed a low night sky quality level, with values between 17.3 and 18.8 MPSAS (Table 2). In contrast, Caleta Hornos, Las Mostazas at Bahía Guanaqueros and central and south Tongoy sectors had the best quality of night sky, with values between 21.0 and 21.4 MPSAS. The values recorded for night sky quality show significant differences among sampling sites (H = 49.76, P = 0.00). A posteriori Tukey analyses distinguished between two groups of sectors, those closest to urban centers and those most distant (Table 3). 3.1.3. Urbanization level The values obtained from the estimated urbanization index fluctuated between 0.11 and 0.94 (Table 4). The lowest
urbanization index values belong to north and south Caleta Hornos, Las Mostazas and south Tongoy, fluctuating within a range of 0.11–0.34. The sectors of Peñuelas, Morrillos, central and north Tongoy have intermediate values between 0.46 and 0.63. The highest urbanization rate values occurred in the sectors of Peñuelas, Playa Changa, south and north La Herradura, with values ranging between 0.8 and 0.94 (Table 4). When the urbanization index was related with the night sky quality values, a significant negative correlation was found (Spearman q, r = 0835, p < 0.05) (Fig. 2), showing that as the level of urbanization increases, the night sky quality decreases. 3.2. Multifactorial ordination of the beaches The MDS plot based on indicators of urbanization recognized three groups of beaches (Fig. 3), which are separated at a Euclidean distance of 2.5. One group consists of the sampling sites located in Bahía La Herradura (north and south), Peñuelas and Playa Changa in Bahia Coquimbo, a second group comprises the sampling sites at Caleta San Pedro, Playa Morrillos at Bahía Guanaqueros and Bahía Tongoy, and the third group consists of the Caleta Hornos and Las Mostazas sectors. 3.3. Abundance of P. maculata The highest average P. maculata abundance (larvae and adults) was recorded in Caleta Hornos (Fig. 4), whereas north La Herradura North and Playa Changa sectors did not register the presence of the beetle. Lower abundances were recorded in Peñuelas and south La Herradura. The P. maculata abundance showed significant differences between the sectors studied (F = 244.90, P = 0.00) (Table 5). Based on an a posteriori Tukey test, there are three groups. The first group consists of the sectors with the highest abundance of P. maculata (48.7 and 21. 7 ind m2). A second group is made up of sectors whose total abundance average varied between 4.4 and 16.3 ind m2, and a third group consists of those sectors with
Please cite this article in press as: González, S.A., et al. Effect of coastal urbanization on sandy beach coleoptera Phaleria maculata (Kulzer, 1959) in northern Chile. Mar. Pollut. Bull. (2014), http://dx.doi.org/10.1016/j.marpolbul.2014.03.042
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S.A. González et al. / Marine Pollution Bulletin xxx (2014) xxx–xxx Table 3 Night sky quality among several sandy beaches along the northern Chilean coast (Kruskal–Wallis and a posteriori Tukey; a = 0.05). Source of Variation
v2
df
p
12 Sectors
49.76
11
*
Tukey test for night sky quality (MPSAS) LHN PCH Mean ranks Non-significance *
17.30
17.52
0.000
P
LHS
CSP
PM
TN
LM
CHS
CHN
TC
TS
18.08
18.82
19.67
20.20
20.57
21.04
21.04
21.10
21.11
2 1.37
Significant value p 6 0.05.
Table 4 Quantification of urbanization indicators (0 corresponds to the total absence and 5 to extremely high level of urbanization) and estimation of urbanization index value on several beaches in the northern Chile coast (see Fig. 1 for sites). CHN
CHS
CSP
P
PCH
LHN
LHS
PM
LM
TN
TC
TS
Proximity to downtown Buildings on the sand Cleaning of the beach Solid waste in the sand Vehicle traffic Night sky quality Demand by visitors
0 0 0 1 1 1 1
1 1 1 1 1 1 1
4 3 0 3 3 2 1
5 4 4 4 3 4 4
5 4 5 5 5 5 2
5 5 5 5 3 5 5
5 5 5 4 3 5 5
3 3 3 2 2 1 2
0 0 1 1 2 1 2
4 4 0 5 5 1 3
3 3 0 5 3 1 2
3 2 0 4 2 0 1
Urbanization index value
0.11
0.20
0.46
0.80
0.89
0.94
0.91
0.46
0.20
0.63
0.49
0.34
Fig. 2. Relationship between urbanization index value and night sky quality for several sandy beaches sampled along the northern Chilean coast (Spearman, a = 0.05; df = 12; r critical value = 0.503) (see Fig. 1 for sites’ locations).
Fig. 3. nMDS ordination plot based on urbanization indicator values for sandy beaches sampled in the Region of Coquimbo, Chile.
2
a lower abundance (0–3.6 ind m ) (Table 5). The proportions of larvae and adults of P. maculata differed between the sectors studied. In south Caleta Hornos, Morrillos, Las Mostazas and Bahía Tongoy sectors the proportion of larvae was higher than adults, whereas in the north Caleta Hornos, Caleta San Pedro and Peñuelas beach, the proportion is reversed and adults are dominant (Fig. 4). The abundance of larvae and adults shows a similar pattern to that observed for the total abundance, with significant differences between the stations studied, but in the case of adult abundance, the a posteriori test separated only two groups of stations (Fig. 4, Table 5). Although there is a trend toward a higher proportion of larvae over adults, this is not constant; for example, in Caleta Hornos, adult abundance far exceeds the abundance of larvae (Fig. 4). 3.4. P. maculata abundance and beach characteristics relationship The mean abundance of larvae, adults and total P. maculata showed a significant positive correlation with the Dean parameter (X) (Spearman q, r = 0.704, p < 0.05; r = 0.690, p < 0.05; r = 0.692, p < 0.05). For other beach characteristics, such as width
(r = 0.053), slope (r = 0.41) and mean grain size (r = 0.04), no significant correlation was found. The relationship between P. maculata abundance (larvae, adults and total) and the urbanization index values obtained for the beach studied shows a negative correlation, which was statistically significant (Spearman q, r = 0893, p < 0.05) (Spearman q, r = 0921, p < 0.05) (Spearman q, r = 0898, p < 0.05). Furthermore, the relationship between the P. maculata abundance and night sky quality demonstrates a significant positive correlation (Spearman q, r = 0.856, p < 0.05) (Spearman q, r = 0.814, p < 0.05) (Spearman q, r = 0.837, p < 0.05) for all sampling sites. Fig. 5 shows the relationship between the MDS ordination – 2D of the 12 sampling sites based on urbanization indicators and the abundance of P. maculata, represented by circles whose diameter is proportional to the abundance of larvae and adults. Comparatively, the ordination showed a clear distinction between different beach urbanization conditions. One group of beach sectors comprised north La Herradura and Playa Changa with high urbanization index levels, which did not register the presence of the beetle, whereas in the south La Herradura and Peñuelas
Please cite this article in press as: González, S.A., et al. Effect of coastal urbanization on sandy beach coleoptera Phaleria maculata (Kulzer, 1959) in northern Chile. Mar. Pollut. Bull. (2014), http://dx.doi.org/10.1016/j.marpolbul.2014.03.042
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S.A. González et al. / Marine Pollution Bulletin xxx (2014) xxx–xxx
Fig. 5. Distribution of Phaleria maculata abundance on nMDS ordination of the sampling sites in the Region of Coquimbo (MDS – 2D) on the basis of indicators of urbanization (ANOVA, F, p < 0.05). The circles represent the mean abundance and proportion of larvae/adults (percentage).
Fig. 4. Abundance of larvae and adults of Phaleria maculata (individuals m2) in several sandy beaches. The black circles on the coastline show the sampling sites. Bars represent the mean abundance and standard error. In the PCH and LHS sites, no individuals were found.
(Bahía Coquimbo), beetle abundance was very low (between 0.1 and 2 ind m2). The prevalence in this group is larvae over adults. A second group of beach sectors with intermediate values of urbanization index comprises Caleta San Pedro in Bahía Coquimbo, Morrillos at Bahía Guanaqueros and Bahía Tongoy, where intermediate abundances of P. maculata and greater predominance of larvae were found, except for Caleta San Pedro. Finally, a third group consisted of Playa Las Mostazas at Bahía Guanaqueros and
Caleta Hornos, presenting the highest abundances of the Coleoptera, including the case of the northern sector of the last beach, which reaches densities that can exceed 30 ind m2, coinciding with the lowest level of urbanization. Adding to this graphical analysis, multiple regression analysis showed a significant relationship between the first two axes of the ordination of sectors from the beach urbanization characteristics obtained through MDS analysis and total abundance (larvae and adults together) with a level of 65% (adjusted r2 0.645; F = 10.99, p = 0.003). 4. Discussion The inverse relationship between the level of urbanization in the northern Chilean beaches and the larval and adult abundance
Table 5 Comparison of the Phaleria maculata abundance (larvae, adults and total) among several sandy beaches (Kruskal–Wallis and a posteriori Tukey; a = 0.05). Phaleria maculata Abundance
v2
df
p
Larvae Adults Total
196.33 111.49 244.90
11 11 11
*
Tukey test on P. maculata larvae (ind m2) PCH LHN Mean ranks Non-significance
0
0
Tukey test on P. maculata adults (ind m2) PCH LHN Mean ranks Non-significance
0
0
*
0
0
*
0.000 0.000 0.000
LHS
P
CSP
PM
TC
TS
TN
LM
CHS
CHN
0.11
0.56
1.56
3.33
3.89
3.33
6.44
11.00
16.78
17.20
LHS
P
PM
CSP
TC
TN
TS
CHS
LM
CHN
0.22
0.67
1.11
2.00
2.56
3.56
3.78
4.89
5.33
31.44
Tukey test on P. maculata (adults + larvae) (ind m2) PCH LHN LHS Mean ranks Non-significance
*
0.33
P
CSP
PM
TC
TS
TN
LM
CHS
CHN
1.22
3.56
4.44
6.44
8.00
10.00
16.33
21.67
48.67
Significant value p 6 0.05.
Please cite this article in press as: González, S.A., et al. Effect of coastal urbanization on sandy beach coleoptera Phaleria maculata (Kulzer, 1959) in northern Chile. Mar. Pollut. Bull. (2014), http://dx.doi.org/10.1016/j.marpolbul.2014.03.042
S.A. González et al. / Marine Pollution Bulletin xxx (2014) xxx–xxx
of the darkling beetle P. maculata, as recorded in this study, confirms the hypothesis that human intervention affects the occurrence of these organisms. Consequently, sectors that recorded high urbanization values showed the absence of the beetle or a presence in very low abundance, whereas sectors with low urbanization levels showed higher Coleoptera abundance. This was also evident in the correlation found between nMDS ordination for urbanization level and the abundance of P. maculata. These results, showing the high sensitivity of this species to environmental changes, suggested that these beetles could be considered as bioindicators of the state of ecosystems of sandy beaches (Fallaci et al., 2002). Some studies have shown that darkling beetles are sensitive to anthropogenic impact (Colombini et al., 2003; Veloso et al., 2006; Comor et al., 2008). It is possible that human intervention affects the abundance of P. maculata via the combined effects of various urbanization factors, including the proximity of buildings to the dunes, the access facilities that contribute to the increase in visitors, debris on the sand, artificial lighting and mechanical beach cleaning. In general, beaches are visited more than any other coastal or marine habitat, so the demand is constantly increasing in use (Schlacher et al., 2007), generating increasing pressure on intertidal fauna populations. For example, in Bahía La Herradura and Playa Changa, the low abundance and even absence of P. maculata may result from the effect of the high concentration of human actions. The calm-water beaches are most demanded by users, compared with rough-water or high-energy beaches. Consequently, these sectors, such as Bahia La Herradura, Playa Changa and Peñuelas, are places that have a high concentration of visitors in summer (SERNATUR, 2012). In addition, habitat alterations suffered by tourist beaches and the high density of visitors walking on the sand can generate different impacts on the environment, such as the destruction of vegetation and fauna, and alterations in the physical characteristics of the beach sand compaction, which subsequently influences soil moisture, erosion, loss of vegetation and the microorganisms that live there (Schlacher and Thompson, 2012). At the top of the beach, the dunes are a natural barrier protecting against the action of the sea and which is also very sensitive to human intervention (Castro, 1987; Dugan and Hubbard, 2010; Noriega et al., 2012). Insects, especially darkling beetles, are particularly sensitive to the characteristics of the places they inhabit (Comor et al., 2008; Colombini et al., 2011). As documented in this study, P. maculata does not tolerate high levels of urbanization, as its abundance decreases dramatically and even disappears in sectors where the urbanization index value was high. Additionally, artificial night lighting usually increases with coastal urbanization. The positive correlation found in this study between night sky quality and abundance of P. maculata confirms previous reports of the detrimental effect of light on locomotor activity of P. maculata (Jaramillo et al., 2000, 2003), and it suggests that this factor is relevant to the ecology of darkling beetles. Further, Giaconni (2006) considered the effect of artificial light to be the primary factor responsible for the decline in abundance of the amphipod Orchestoidea tuberculata in the area studied. Intertidal fauna, such as insects, amphipods and isopods, require darkness to complete their daily cycles, to use astronomical signals and to move back to their burrows in the upper part of the beach (Fallaci et al., 2002). Considering the increase in coastal urbanization, more studies specifically evaluating the effects of night lighting on beach fauna (‘‘ecological light pollution’’ sensu Longcore and Rich (2004)) are required for establishing more regulations to protect natural communities (Smith, 2009; Deplegde et al., 2010; Gaston et al., 2012). Moreover, the relationship found in this study suggests that the measurement of the night sky quality could be used as an indicator of urbanization.
7
The urbanization index proposal for the northern Chilean coast adequately represents the development level for the sandy beaches studied and was significantly correlated with the abundance of P. maculata, showing an inverse correlation. Measuring the level of urbanization or anthropization through this index, based on the integration of a set of human actions that characterize the process of urbanization of sandy beaches, allows quick and simple semi-quantitative estimation for each location. Similarly, Martínez-Dueñas (2004, 2010) has studied the level of human impact on terrestrial beetles using a relative integrated anthropization index in relation to the different use-coverages of an area, allowing a quantitative measurement of the spatial variation of human impact. Northern Chile has extensive coastlines, as yet unreached by the intense development found along the central coast, so this type of easily applied comparative index can help generate scientific information about the impact of human activities and help set conservation objectives. Nevertheless, in Caleta Hornos and Playa Las Mostazas, the abundance of P. maculata was significantly higher than in the other sectors studied, with a relatively high Dean parameter, which coincides with areas that have a very low level of human intervention. In sectors with lower energy, such as Caleta San Pedro, Peñuelas and Tongoy, the abundance of P. maculata was lower, while in Playa Changa in Bahía Coquimbo and north Bahía La Herradura, where the parameter value from the beach morphodynamic was minimal and further development of these sectors is extremely high, the darkling beetle was apparently absent. These differences could be interpreted from the perspective of the beach morphodynamics, which considers that dissipative beaches would harbor a greater diversity and abundance of organisms in relation to reflective beaches (Veloso et al., 2006). However, it should be noted that beaches with lower Dean values are beaches that are more ‘‘attractive’’ for tourist activities. Beaches in Bahía Coquimbo and Bahía La Herradura receive a high load of visitors in summer and are also subjected to mechanical cleaning and even sometimes the removal of algae stranded on the shore by the use of mechanical plows (Loyola, 2012). Both bays have shown massive tourism development during the last 10 years, with a high occupancy of the dunes for construction of different entertainment and accommodation services, whose impact on natural communities has not been evaluated. Although the impacts are not immediately visible, as explained by Schlacher and Thompson (2012), the ramifications of the impact that human activities can have on the macrobenthos are wide and can affect the functions of sandy beach ecosystems. In northern Chile, P. maculata is located in the high tide fringe, called the ‘‘drying zone’’, where it is accompanied by Excirolana braziliensis (Jaramillo et al., 1998); in the areas sampled in this study, we also found it sharing space with O. tuberculata. Although these two species of crustaceans have been described as the most abundant in the upper intertidal sandy Chilean coast, they are smaller in body size than P. maculata, such that their biomass can far exceed their contribution to organic matter in the beach ecosystem. P. maculata larvae can reach sizes close to 20 mm, and adults are approximately 10 mm in size; the average weight is approximately 0.05 g for the adult and approximately 0.02 g for larvae (Vega et al., 2007). Considering the average weight and density of Coleoptera recorded in this study, the biomass of P. maculata may reach high values, such as at Caleta Hornos, where the biomass would be estimated at 2 g m2. These values are significant for the highest fringe of the beach, where available organic matter is very low. P. maculata abundance in this study (max. approx. 50 individuals m2) reached higher values than recorded in other places, such as the beaches of Portugal (
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Marine Pollution Bulletin journal homepage: www.elsevier.com/locate/marpolbul
Effect of coastal urbanization on sandy beach coleoptera Phaleria maculata (Kulzer, 1959) in northern Chile Sergio A. González ⇑, Katherine Yáñez-Navea, Mauricio Muñoz Departamento de Biología Marina, Facultad de Ciencias del Mar, Universidad Católica del Norte, Casilla 117, Coquimbo, Chile
a r t i c l e
i n f o
Keywords: Marine tenebrionid Phaleria maculata Anthropogenic impact Coastal urbanization index Light pollution
a b s t r a c t The beetle Phaleria maculata is a common inhabitant of the upper intertidal fringe of Chilean beaches. Anthropogenic intervention in coastal areas has increased intensely, leading to changes in the flora and fauna of sandy beaches. To examine the impact of human activities on P. maculata, we studied several beaches along the northern Chilean coast. Beaches were characterized based on morphodynamics and the level of intervention, leading to the estimation of an ‘‘Urbanization Index’’ based on various indicators. The analysis showed a significant inverse correlation between the rate of urbanization and night sky quality. Larval and adult beetles were almost absent on beaches with high levels of urbanization. The results of simple and multiple correlations based on nMDS ordination showed an inverse relationship between increases in urbanization and the abundance of beetles. Because darkling beetles are very sensitive to human interventions on sandy beaches, we suggest that they are ideal indicator organisms for the health of these environments. Ó 2014 Elsevier Ltd. All rights reserved.
1. Introduction The growing human pressure on natural systems results in strong impacts, some of which may be irreversible. Halpern et al. (2008) noted that at present, all marine ecosystems have been affected by human activities, especially in the coastal zone. In the case of Latin America, a classification based on an estimate of a Threat Index has shown that the coasts of Brazil, Peru and Ecuador are subject to the greatest impacts (Chatwin and Rybock, 2007). The major threats to biodiversity in South America are fisheries, pollution, urbanization, mining, the oil industry, aquaculture, shipping, invasive species, and climate change. Among these threats, the urbanization of the coastal zone in parts of Latin America has been very rapid, following the regional economic boom and leading to ‘‘sun and beach tourism’’. The high demand for seaside spaces, lack of institutional experience with handling this demand and the limitations of scientific knowledge on the dynamics of coastal ecosystems and the impacts on natural systems have been identified as major factors causing deterioration of coastal environments (Dayton, 2003; Orams, 2003; Dias et al., 2012). In general,
⇑ Corresponding author. Address: Departamento de Biología Marina, Facultad de Ciencias del Mar, Universidad Católica del Norte (UCN), Larrondo 1281, Casilla 117, Coquimbo, Chile. Tel.: +56 51 2209786; fax: +56 51 2209812. E-mail address: [email protected] (S.A. González).
coastal ecosystems are very sensitive to the impacts associated with mass tourism (Dadon, 2002). As more and more beaches are urbanized, natural resources become more valuable not only for permanent residents but also for tourists looking for pristine beaches and clear waters, clean air and natural sounds, among other features (Roca and Villares, 2008; Roca et al., 2009). In recent decades, human impacts on sandy beaches have strongly increased, resulting in a significant alteration of their flora and fauna (Brown and McLachlan, 2002; Schlacher et al., 2007, 2008; Defeo et al., 2009). Globally, many of the sandy beaches close to urban areas have undergone complete removal of landward dunes due to construction of roads and buildings (Morteiro and Bemvenuti, 2006), dramatically transforming these environments. The pursuit of economic growth through the exploitation of recreation and tourism on beaches has generated intensive urban growth, resulting in major disruptions to natural communities by intense trampling of fragile sandy beach habitats during the summer (Comor et al., 2008), the incorporation of solid waste (Thiel et al., 2003; Bravo et al., 2009), and the passage of vehicles (Gheskiere et al., 2006; Veloso et al., 2008). Moreover, the intense use of sandy beaches as recreational sites and the growing demand for ‘‘quality’’ by the users have forced local authorities in many countries to mechanically remove flotsam (natural and anthropogenic) from beaches, further altering the natural habitat (Ryan and Swanepoel, 1996; Defeo et al., 2009; MacLachlan et al., 2013). Human activities in many highly touristic
http://dx.doi.org/10.1016/j.marpolbul.2014.03.042 0025-326X/Ó 2014 Elsevier Ltd. All rights reserved.
Please cite this article in press as: González, S.A., et al. Effect of coastal urbanization on sandy beach coleoptera Phaleria maculata (Kulzer, 1959) in northern Chile. Mar. Pollut. Bull. (2014), http://dx.doi.org/10.1016/j.marpolbul.2014.03.042
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S.A. González et al. / Marine Pollution Bulletin xxx (2014) xxx–xxx
areas require lighting, resulting in dense coverage of artificial lights along these beaches, which not only affects the natural habitats but also leads to a gradual ‘‘disappearance’’ of starlight (Smith, 2009). Consequently, many coastal habitats, communities and ecosystems are exposed year-round to the impact of artificial light (Longcore and Rich, 2004; Navara and Nelson, 2007; Hölker et al., 2010). This relationship between artificial night lighting and human development has been an indicator of levels of urbanization in the fields of economics and remote-sensing engineering (Ghosh et al., 2010; Ma et al., 2012; Zhang and Seto, 2013), but it has received little attention from marine ecologists. Although little studied, tenebrionid beetles are common organisms on sandy beaches, being described as ‘‘sensitive’’ to environmental perturbations (Veloso et al., 2008; Comor et al., 2008). These organisms are dominant in the upper part of the beach, presenting morphological and ecophysiological adaptations that confer resistance to lack of freshwater and to high temperatures (Colombini et al., 1994). Due to the high biomass of local beetle populations (larvae and adults) on sandy beaches, they play a key ecological role in coastal environments, facilitating the processes of fragmentation and decomposition of plant and animal remains, as well as the activation of nutrient cycles, particularly in those ecosystems where microbial action is restricted due to low humidity (Santos et al., 1988; Cepeda-Pizarro, 1989; Cartagena et al., 2002). These beetles also play an important ecological role as mobilizers of matter and energy between the marine and terrestrial ecosystems (Cheng, 1976). On the Pacific coast of South America, adults and larval stages of Phaleria maculata (Kulzer, 1959) (formerly Phalerisida maculata) can be commonly found under kelp debris and other organic matter stranded in the supralittoral fringe of the beach (Peña, 1996; Vidal and Guerrero, 2007). In Chile, there have been various studies of sandy beaches (Hernández et al., 1998; Contreras and Jaramillo, 2003), but the ecological role of these organisms is poorly known (Avellanal et al., 2000; Jaramillo et al., 2003, 2006). Like other countries in Latin America, the Chilean government is making efforts to promote tourism (Barragán, 2001; Santana, 2003). Various coastal administrations in north-central Chile have based their economic development on tourism, which has involved a greater degree of building both recreational and residential structures in close proximity to the beaches. This increasing urbanization may affect the fauna of the beach, but this has not yet been evaluated. For this reason, the present study assesses the level and effect of various factors related to urbanization on the abundance of the marine darkling beetle P. maculata along a stretch of coast in the Region of Coquimbo, in northern Chile. We test the hypothesis that intensive coastal development causes a decrease in the abundance of these beetles.
2. Methods 2.1. Study area Twelve sandy beach locations were sampled along 100 km of the Coquimbo seashore in northern Chile (Fig. 1). The sampling sites show different degrees of urbanization. Some beaches, La Herradura, Changa, northern Tongoy and Peñuelas, are integrated into the city, where they are in high tourist demand and close to paved roads that include night lighting, kiosks selling food, residential buildings and high-rise buildings. In summer, there is a clear increase in the amount of solid waste in the sand because of the high presence of visitors, such that municipal administrators rake the beach with heavy machinery. Other beaches, such as Caleta Hornos, Morrillos, Las Mostazas and southern Tongoy, are far from
urban centers, where the level of intervention is low compared to urban beaches.
2.2. Physical characterization The beach slope of each location was estimated from the height difference between the drift line and water line (Emery, 1961). To estimate the morphodynamic state of the beach, the Dean parameter (X) (Wright and Short, 1984) was used; three samples of sediment were collected at the drift line, separated by approximately 50 m, using a core of 4 cm in diameter which was buried up to 15 cm. Particle size and average grain size were determined using a settling tube. The sedimentation rate of the particles was evaluated based on tables from Gibbs et al. (1971) on the basis of the calculation of average particle size using the ‘‘computational method of moments’’ (Seward-Thompson and Hails, 1973). The wave height was estimated using a centimeter ruler and aligned with the horizon, for 10 waves on each of three occasions separated by approximately 30–45 min. The period of the wave, considered as the elapsed time (seconds) between two waves that break, was measured on three occasions separated by 30–45 min, using a digital stopwatch to count the waves that occurred in 5 min.
2.3. Urbanization level The level of urbanization was estimated by calculating an index with 7 variables: (1) Proximity to urban centers, (2) Building on the sand, (3) Beach cleaning, (4) Solid waste on the sand, (5) Vehicle traffic on the sand, (6) Quality of the night sky, and (7) Frequency of visitors. These indicators were systematized through a rubric featuring low, medium, and high ‘‘levels of development’’ (Table 1). In turn, each level was divided into two scores (0–1, 2–3 and 4–5) to give greater certainty to the estimate, ‘‘0’’ could be indicated in the case of the complete absence of the variable estimated, versus ‘‘5’’ when extremely high levels were observed. The level of proximity to the city and the presence of buildings, solid waste on the sand and traces of vehicle traffic were estimated by direct observation in the field. The night sky quality was assessed using magnitude charts for the nighttime sky from the NOAO ‘‘Globe at Night’’ Program as reference (www.globeatnight.org). For beach cleaning and frequency of visitors, in addition to field observations, information provided by the National Tourism Service (SERNATUR Chile) and Municipal Administrators was considered. Urbanization index was calculated using the method of Gover, X0 = ((X–Xmin)/(Xmax–Xmin)) (Legendre and Legendre, 1998), which reduced the indicator values to a range [0–1]; where X is the value assigned to each of the seven variables and Xmin–Xmax corresponds to the extreme values of the range (0–5 in this case). Index values ranking close to ‘‘0’’ indicating beaches with low human intervention and sectors with values close to ‘‘1’’ indicating beaches with high human intervention. Additionally, to evaluate the relationship between this index and the night lighting, the night sky quality was determined using SQM-L (Sky Quality Meter). For this case, 5 measurements were taken at each point at different angles of orientation toward the sky. The SQM-L allows objective measurements of the quality of the sky, incorporating a highly sensitive photometer that measures the brightness of the sky (only visible light) at a particular angle of the sky. The data were expressed on a logarithmic scale of magnitudes per square arcsecond (MPSAS), which ranges from a value of 17 for highly polluted skies and 23 for dark skies (visit http://unihedron.com for more details). To reduce variations, the measurements were made over a period of two consecutive days with clear skies and at 23:00 h.
Please cite this article in press as: González, S.A., et al. Effect of coastal urbanization on sandy beach coleoptera Phaleria maculata (Kulzer, 1959) in northern Chile. Mar. Pollut. Bull. (2014), http://dx.doi.org/10.1016/j.marpolbul.2014.03.042
S.A. González et al. / Marine Pollution Bulletin xxx (2014) xxx–xxx
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Fig. 1. Locations of 12 studied beaches in the IV Región de Coquimbo, northern Chilean coast. CHN = North and CHS = South side of Caleta Hornos; CSP = Caleta San Pedro; P = Caleta Peñuelas; PCH = Playa Changa; LHN = North and LHS = South side of Bahía La Herradura; PM = Playa Morrillos; LM = Playa Las Mostazas, and TN = North, TC = Center and TS = South side of Bahía Tongoy.
2.4. Abundance of P. maculata Although the zonation of sandy beach macroinfauna has been described for Chile (Jaramillo, 1987), a systematic and intensive beach-level sampling design was used (James and Fairweather, 1996) where the beetle population is concentrated (Jaramillo et al., 1993; Jaramillo et al., 2006). At each study site, the abundance of P. maculata larvae and adults was recorded at 3 sampling stations separated by 50 m. At each sampling station, 10 transects were established perpendicular to the coastline and separated by 1.5 m. Each transect had 3 levels, one higher than 1.5 m above the drift line, a medium level exactly on the drift line, and a low level located 1.5 m below the drift line. This involved a total of 30 samples per station and 90 samples in total per sector. Larvae and adults of P. maculata were collected with a core of 0.1 m that was buried 20 cm in the sand. The sample was sifted using 1-mm mesh and then carried to the water to remove sand and thereby collect fauna, which were fixed with a solution of 70% alcohol in seawater. Samples were analyzed in the laboratory for the quantification of larvae and adults. 2.5. Analysis Possible differences in the abundance of P. maculata (larvae, adults and total) between the beaches sampled were studied using non-parametric analysis of k independent samples with the Kruskal–Wallis test (H, P = 0.05) because not all of the assumptions required by parametric tests were met. The same statistical analysis was used to assess the significance of differences in morphometric characteristics and the quality of night sky between the beaches studied. An a posteriori Tukey test was used to discriminate between the beaches studied when differences were significant. The correlation between the mean abundance of P. maculata (larvae, adults and total) and the characteristics of the sampled sites (geomorphological characteristics, urbanization index, and night sky quality) were evaluated by Spearman non-parametric
correlation analysis, and the significance was evaluated based the critical value of ‘‘r’’ at a level of 0.05 (Zar, 1999) using SPSS 17. To provide an integrative approach and only for comparative purposes, the abundance of P. maculata (adults, larvae and total) was plotted on the MDS ordination – 2D sampling sites based on human intervention variables used to estimate the ‘‘urbanization index’’. This ordination was made using a Euclidean distance matrix using transformed data (log x + 1) and subsequently grouped using the UPGMA technique, in the statistical program Past. Subsequently, to obtain a measure of this relationship, the values of the first two dimensions of the MDS plot that grouped the sampling sites were compared with the P. maculata mean abundance using a multiple regression analysis. The significance of the value of r2 was assessed by ANOVA (F, P < 0.05) (Zar, 1999). 3. Results 3.1. Beach characteristics 3.1.1. Morphodynamics The sampled areas showed varying characteristics, from beaches that had an approximate width of 26 m in Caleta San Pedro to the case of south Caleta Hornos, which featured a beach of approximately 63 m wide. Similarly, the beach slope ranged from 1°, as with Playa Peñuelas, up to more than 5°, as in Las Mostazas. The mean recorded values for grain size corresponded to medium sand, with the exception of south Caleta Hornos, Caleta San Pedro, Peñuelas and north La Herradura, which showed fine sand. Of the morphodynamic states of the sampled sites, Caleta Hornos and Caleta San Pedro beaches are intermediate in character (1 < X < 6), with a moderate energy. However, the south Caleta Hornos showed increased wave height compared with the other areas of study. The beaches Peñuelas, Changa, La Herradura, Morrillos, Las Mostazas and Tongoy were classified as reflective beaches (X < 1), with low energy. However, in this category, Playa Changa and Bahía La Herradura, both northern and southern sectors, presented the lowest values of the Dean’s parameter (Table 2). Only
Please cite this article in press as: González, S.A., et al. Effect of coastal urbanization on sandy beach coleoptera Phaleria maculata (Kulzer, 1959) in northern Chile. Mar. Pollut. Bull. (2014), http://dx.doi.org/10.1016/j.marpolbul.2014.03.042
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Table 1 Qualitative indicators of human intervention used in estimating the level of beach urbanization in northern Chile. Beach urbanization indicator levels Low 0–1
Medium 2–3
High 4–5
Proximity to urban centers Buildings on the sand
Sector with rural character. Several kilometers away from urban center. No direct influence of an urban center on the beach No nearby buildings appreciable
Sector located c. 1 km from an urban center, showing some effects on the beach, such as noise, some lighting and nearby vehicles passing
Sector just meters from an urban center, the city virtually integrated. The beach is next to vehicular traffic, with evident noise and urban lighting
There are buildings close to the beach but not on the sand or the dunes
There are buildings that occupy the space at the beach or in the dunes
Cleaning of the beach
The beach is not ‘‘cleaned’’ by mechanical means, with no sand removal
Although mechanically engaged for cleaning, this is done infrequently, no more than 1 time per week. No frequent removal of sand
Beach is repeatedly cleaned by mechanical means, more than once a week, which causes frequent removal of the sand
Solid waste in the sand
No waste in the sand or the amount of waste on the beach is minimal
In a short walk of a few meters, some solid waste can be seen on the sand, such as paper, plastic containers and cigarette butts
Clearly a high frequency of solid waste on the sand, including papers, plastic containers, cigarette butts, plastic debris, scrap wood and glass
Vehicles traffic on the sand
No vehicle tracks were observed on the sand. There is no vehicle access on the beach
Although there are traces of vehicle passage, they are scarce. Vehicular crossing is not periodic and not constant. Vehicular access to the beach is relatively limited
There are many tracks, showing recurring vehicular traffic. Various vehicles have access to the beach
Quality of the night sky
Sky conditions are optimal for stargazing. The sky appears black, and hundreds of stars can be seen perfectly
The glow of artificial light moderately impaired conditions for stargazing. The sky appears dark gray, and some tens of stars can be seen with some difficulty
Given the high brightness of the artificial lighting, the conditions for stargazing are bad. The sky is gray and occasional stars can be seen. Light pollution is evident
Frequency of visitors
The area is visited by very few people, and those are located in areas isolated from each other. Rural beach
The sector has a moderate demand for use. Although it has tourists, based on either location or privacy, it does not have a large number of users
Sector in high demand from users, considered a high tourist beach. Public access urban beach
Table 2 Characterization of the study sites in terms of sand grain size, beach morphodynamics and night sky quality. Beach sampling locations
Mean grain size (mm) ðX_ SDÞ
Dean’s parameter (X)
Night sky quality (MPSAS) ðX_ SDÞ
North Caleta Hornos South Caleta Hornos Caleta San Pedro Peñuelas Playa Changa North La Herradura South La Herradura Morrillos Las Mostazas North Tongoy Central Tongoy South Tongoy
0.34 ± 0.030 0.18 ± 0.028 0.25 ± 0.034 0.20 ± 0.021 0.37 ± 0.022 0.22 ± 0.031 0.31 ± 0.048 0.35 ± 0.015 0.37 ± 0.020 0.31 ± 0.003 0.35 ± 0.026 0.29 ± 0.004
3.49 5.26 2.19 0.46 0.10 0.09 0.07 0.75 0.63 0.32 0.20 0.40
21.10 ± 0.35 21.04 ± 0.34 19.67 ± 0.55 18.08 ± 1.30 17.52 ± 1.65 17.30 ± 1.46 18.82 ± 0.51 20.20 ± 0.25 21.04 ± 0.22 20.57 ± 0.57 21.11 ± 0.37 21.37 ± 0.14
X showed significant differences among sampling sites (H = 61.930, P = 0.00); the other variables did not differ among the beaches. 3.1.2. Night sky quality The areas of north and south La Herradura, Playa Changa and Peñuelas showed a low night sky quality level, with values between 17.3 and 18.8 MPSAS (Table 2). In contrast, Caleta Hornos, Las Mostazas at Bahía Guanaqueros and central and south Tongoy sectors had the best quality of night sky, with values between 21.0 and 21.4 MPSAS. The values recorded for night sky quality show significant differences among sampling sites (H = 49.76, P = 0.00). A posteriori Tukey analyses distinguished between two groups of sectors, those closest to urban centers and those most distant (Table 3). 3.1.3. Urbanization level The values obtained from the estimated urbanization index fluctuated between 0.11 and 0.94 (Table 4). The lowest
urbanization index values belong to north and south Caleta Hornos, Las Mostazas and south Tongoy, fluctuating within a range of 0.11–0.34. The sectors of Peñuelas, Morrillos, central and north Tongoy have intermediate values between 0.46 and 0.63. The highest urbanization rate values occurred in the sectors of Peñuelas, Playa Changa, south and north La Herradura, with values ranging between 0.8 and 0.94 (Table 4). When the urbanization index was related with the night sky quality values, a significant negative correlation was found (Spearman q, r = 0835, p < 0.05) (Fig. 2), showing that as the level of urbanization increases, the night sky quality decreases. 3.2. Multifactorial ordination of the beaches The MDS plot based on indicators of urbanization recognized three groups of beaches (Fig. 3), which are separated at a Euclidean distance of 2.5. One group consists of the sampling sites located in Bahía La Herradura (north and south), Peñuelas and Playa Changa in Bahia Coquimbo, a second group comprises the sampling sites at Caleta San Pedro, Playa Morrillos at Bahía Guanaqueros and Bahía Tongoy, and the third group consists of the Caleta Hornos and Las Mostazas sectors. 3.3. Abundance of P. maculata The highest average P. maculata abundance (larvae and adults) was recorded in Caleta Hornos (Fig. 4), whereas north La Herradura North and Playa Changa sectors did not register the presence of the beetle. Lower abundances were recorded in Peñuelas and south La Herradura. The P. maculata abundance showed significant differences between the sectors studied (F = 244.90, P = 0.00) (Table 5). Based on an a posteriori Tukey test, there are three groups. The first group consists of the sectors with the highest abundance of P. maculata (48.7 and 21. 7 ind m2). A second group is made up of sectors whose total abundance average varied between 4.4 and 16.3 ind m2, and a third group consists of those sectors with
Please cite this article in press as: González, S.A., et al. Effect of coastal urbanization on sandy beach coleoptera Phaleria maculata (Kulzer, 1959) in northern Chile. Mar. Pollut. Bull. (2014), http://dx.doi.org/10.1016/j.marpolbul.2014.03.042
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S.A. González et al. / Marine Pollution Bulletin xxx (2014) xxx–xxx Table 3 Night sky quality among several sandy beaches along the northern Chilean coast (Kruskal–Wallis and a posteriori Tukey; a = 0.05). Source of Variation
v2
df
p
12 Sectors
49.76
11
*
Tukey test for night sky quality (MPSAS) LHN PCH Mean ranks Non-significance *
17.30
17.52
0.000
P
LHS
CSP
PM
TN
LM
CHS
CHN
TC
TS
18.08
18.82
19.67
20.20
20.57
21.04
21.04
21.10
21.11
2 1.37
Significant value p 6 0.05.
Table 4 Quantification of urbanization indicators (0 corresponds to the total absence and 5 to extremely high level of urbanization) and estimation of urbanization index value on several beaches in the northern Chile coast (see Fig. 1 for sites). CHN
CHS
CSP
P
PCH
LHN
LHS
PM
LM
TN
TC
TS
Proximity to downtown Buildings on the sand Cleaning of the beach Solid waste in the sand Vehicle traffic Night sky quality Demand by visitors
0 0 0 1 1 1 1
1 1 1 1 1 1 1
4 3 0 3 3 2 1
5 4 4 4 3 4 4
5 4 5 5 5 5 2
5 5 5 5 3 5 5
5 5 5 4 3 5 5
3 3 3 2 2 1 2
0 0 1 1 2 1 2
4 4 0 5 5 1 3
3 3 0 5 3 1 2
3 2 0 4 2 0 1
Urbanization index value
0.11
0.20
0.46
0.80
0.89
0.94
0.91
0.46
0.20
0.63
0.49
0.34
Fig. 2. Relationship between urbanization index value and night sky quality for several sandy beaches sampled along the northern Chilean coast (Spearman, a = 0.05; df = 12; r critical value = 0.503) (see Fig. 1 for sites’ locations).
Fig. 3. nMDS ordination plot based on urbanization indicator values for sandy beaches sampled in the Region of Coquimbo, Chile.
2
a lower abundance (0–3.6 ind m ) (Table 5). The proportions of larvae and adults of P. maculata differed between the sectors studied. In south Caleta Hornos, Morrillos, Las Mostazas and Bahía Tongoy sectors the proportion of larvae was higher than adults, whereas in the north Caleta Hornos, Caleta San Pedro and Peñuelas beach, the proportion is reversed and adults are dominant (Fig. 4). The abundance of larvae and adults shows a similar pattern to that observed for the total abundance, with significant differences between the stations studied, but in the case of adult abundance, the a posteriori test separated only two groups of stations (Fig. 4, Table 5). Although there is a trend toward a higher proportion of larvae over adults, this is not constant; for example, in Caleta Hornos, adult abundance far exceeds the abundance of larvae (Fig. 4). 3.4. P. maculata abundance and beach characteristics relationship The mean abundance of larvae, adults and total P. maculata showed a significant positive correlation with the Dean parameter (X) (Spearman q, r = 0.704, p < 0.05; r = 0.690, p < 0.05; r = 0.692, p < 0.05). For other beach characteristics, such as width
(r = 0.053), slope (r = 0.41) and mean grain size (r = 0.04), no significant correlation was found. The relationship between P. maculata abundance (larvae, adults and total) and the urbanization index values obtained for the beach studied shows a negative correlation, which was statistically significant (Spearman q, r = 0893, p < 0.05) (Spearman q, r = 0921, p < 0.05) (Spearman q, r = 0898, p < 0.05). Furthermore, the relationship between the P. maculata abundance and night sky quality demonstrates a significant positive correlation (Spearman q, r = 0.856, p < 0.05) (Spearman q, r = 0.814, p < 0.05) (Spearman q, r = 0.837, p < 0.05) for all sampling sites. Fig. 5 shows the relationship between the MDS ordination – 2D of the 12 sampling sites based on urbanization indicators and the abundance of P. maculata, represented by circles whose diameter is proportional to the abundance of larvae and adults. Comparatively, the ordination showed a clear distinction between different beach urbanization conditions. One group of beach sectors comprised north La Herradura and Playa Changa with high urbanization index levels, which did not register the presence of the beetle, whereas in the south La Herradura and Peñuelas
Please cite this article in press as: González, S.A., et al. Effect of coastal urbanization on sandy beach coleoptera Phaleria maculata (Kulzer, 1959) in northern Chile. Mar. Pollut. Bull. (2014), http://dx.doi.org/10.1016/j.marpolbul.2014.03.042
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S.A. González et al. / Marine Pollution Bulletin xxx (2014) xxx–xxx
Fig. 5. Distribution of Phaleria maculata abundance on nMDS ordination of the sampling sites in the Region of Coquimbo (MDS – 2D) on the basis of indicators of urbanization (ANOVA, F, p < 0.05). The circles represent the mean abundance and proportion of larvae/adults (percentage).
Fig. 4. Abundance of larvae and adults of Phaleria maculata (individuals m2) in several sandy beaches. The black circles on the coastline show the sampling sites. Bars represent the mean abundance and standard error. In the PCH and LHS sites, no individuals were found.
(Bahía Coquimbo), beetle abundance was very low (between 0.1 and 2 ind m2). The prevalence in this group is larvae over adults. A second group of beach sectors with intermediate values of urbanization index comprises Caleta San Pedro in Bahía Coquimbo, Morrillos at Bahía Guanaqueros and Bahía Tongoy, where intermediate abundances of P. maculata and greater predominance of larvae were found, except for Caleta San Pedro. Finally, a third group consisted of Playa Las Mostazas at Bahía Guanaqueros and
Caleta Hornos, presenting the highest abundances of the Coleoptera, including the case of the northern sector of the last beach, which reaches densities that can exceed 30 ind m2, coinciding with the lowest level of urbanization. Adding to this graphical analysis, multiple regression analysis showed a significant relationship between the first two axes of the ordination of sectors from the beach urbanization characteristics obtained through MDS analysis and total abundance (larvae and adults together) with a level of 65% (adjusted r2 0.645; F = 10.99, p = 0.003). 4. Discussion The inverse relationship between the level of urbanization in the northern Chilean beaches and the larval and adult abundance
Table 5 Comparison of the Phaleria maculata abundance (larvae, adults and total) among several sandy beaches (Kruskal–Wallis and a posteriori Tukey; a = 0.05). Phaleria maculata Abundance
v2
df
p
Larvae Adults Total
196.33 111.49 244.90
11 11 11
*
Tukey test on P. maculata larvae (ind m2) PCH LHN Mean ranks Non-significance
0
0
Tukey test on P. maculata adults (ind m2) PCH LHN Mean ranks Non-significance
0
0
*
0
0
*
0.000 0.000 0.000
LHS
P
CSP
PM
TC
TS
TN
LM
CHS
CHN
0.11
0.56
1.56
3.33
3.89
3.33
6.44
11.00
16.78
17.20
LHS
P
PM
CSP
TC
TN
TS
CHS
LM
CHN
0.22
0.67
1.11
2.00
2.56
3.56
3.78
4.89
5.33
31.44
Tukey test on P. maculata (adults + larvae) (ind m2) PCH LHN LHS Mean ranks Non-significance
*
0.33
P
CSP
PM
TC
TS
TN
LM
CHS
CHN
1.22
3.56
4.44
6.44
8.00
10.00
16.33
21.67
48.67
Significant value p 6 0.05.
Please cite this article in press as: González, S.A., et al. Effect of coastal urbanization on sandy beach coleoptera Phaleria maculata (Kulzer, 1959) in northern Chile. Mar. Pollut. Bull. (2014), http://dx.doi.org/10.1016/j.marpolbul.2014.03.042
S.A. González et al. / Marine Pollution Bulletin xxx (2014) xxx–xxx
of the darkling beetle P. maculata, as recorded in this study, confirms the hypothesis that human intervention affects the occurrence of these organisms. Consequently, sectors that recorded high urbanization values showed the absence of the beetle or a presence in very low abundance, whereas sectors with low urbanization levels showed higher Coleoptera abundance. This was also evident in the correlation found between nMDS ordination for urbanization level and the abundance of P. maculata. These results, showing the high sensitivity of this species to environmental changes, suggested that these beetles could be considered as bioindicators of the state of ecosystems of sandy beaches (Fallaci et al., 2002). Some studies have shown that darkling beetles are sensitive to anthropogenic impact (Colombini et al., 2003; Veloso et al., 2006; Comor et al., 2008). It is possible that human intervention affects the abundance of P. maculata via the combined effects of various urbanization factors, including the proximity of buildings to the dunes, the access facilities that contribute to the increase in visitors, debris on the sand, artificial lighting and mechanical beach cleaning. In general, beaches are visited more than any other coastal or marine habitat, so the demand is constantly increasing in use (Schlacher et al., 2007), generating increasing pressure on intertidal fauna populations. For example, in Bahía La Herradura and Playa Changa, the low abundance and even absence of P. maculata may result from the effect of the high concentration of human actions. The calm-water beaches are most demanded by users, compared with rough-water or high-energy beaches. Consequently, these sectors, such as Bahia La Herradura, Playa Changa and Peñuelas, are places that have a high concentration of visitors in summer (SERNATUR, 2012). In addition, habitat alterations suffered by tourist beaches and the high density of visitors walking on the sand can generate different impacts on the environment, such as the destruction of vegetation and fauna, and alterations in the physical characteristics of the beach sand compaction, which subsequently influences soil moisture, erosion, loss of vegetation and the microorganisms that live there (Schlacher and Thompson, 2012). At the top of the beach, the dunes are a natural barrier protecting against the action of the sea and which is also very sensitive to human intervention (Castro, 1987; Dugan and Hubbard, 2010; Noriega et al., 2012). Insects, especially darkling beetles, are particularly sensitive to the characteristics of the places they inhabit (Comor et al., 2008; Colombini et al., 2011). As documented in this study, P. maculata does not tolerate high levels of urbanization, as its abundance decreases dramatically and even disappears in sectors where the urbanization index value was high. Additionally, artificial night lighting usually increases with coastal urbanization. The positive correlation found in this study between night sky quality and abundance of P. maculata confirms previous reports of the detrimental effect of light on locomotor activity of P. maculata (Jaramillo et al., 2000, 2003), and it suggests that this factor is relevant to the ecology of darkling beetles. Further, Giaconni (2006) considered the effect of artificial light to be the primary factor responsible for the decline in abundance of the amphipod Orchestoidea tuberculata in the area studied. Intertidal fauna, such as insects, amphipods and isopods, require darkness to complete their daily cycles, to use astronomical signals and to move back to their burrows in the upper part of the beach (Fallaci et al., 2002). Considering the increase in coastal urbanization, more studies specifically evaluating the effects of night lighting on beach fauna (‘‘ecological light pollution’’ sensu Longcore and Rich (2004)) are required for establishing more regulations to protect natural communities (Smith, 2009; Deplegde et al., 2010; Gaston et al., 2012). Moreover, the relationship found in this study suggests that the measurement of the night sky quality could be used as an indicator of urbanization.
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The urbanization index proposal for the northern Chilean coast adequately represents the development level for the sandy beaches studied and was significantly correlated with the abundance of P. maculata, showing an inverse correlation. Measuring the level of urbanization or anthropization through this index, based on the integration of a set of human actions that characterize the process of urbanization of sandy beaches, allows quick and simple semi-quantitative estimation for each location. Similarly, Martínez-Dueñas (2004, 2010) has studied the level of human impact on terrestrial beetles using a relative integrated anthropization index in relation to the different use-coverages of an area, allowing a quantitative measurement of the spatial variation of human impact. Northern Chile has extensive coastlines, as yet unreached by the intense development found along the central coast, so this type of easily applied comparative index can help generate scientific information about the impact of human activities and help set conservation objectives. Nevertheless, in Caleta Hornos and Playa Las Mostazas, the abundance of P. maculata was significantly higher than in the other sectors studied, with a relatively high Dean parameter, which coincides with areas that have a very low level of human intervention. In sectors with lower energy, such as Caleta San Pedro, Peñuelas and Tongoy, the abundance of P. maculata was lower, while in Playa Changa in Bahía Coquimbo and north Bahía La Herradura, where the parameter value from the beach morphodynamic was minimal and further development of these sectors is extremely high, the darkling beetle was apparently absent. These differences could be interpreted from the perspective of the beach morphodynamics, which considers that dissipative beaches would harbor a greater diversity and abundance of organisms in relation to reflective beaches (Veloso et al., 2006). However, it should be noted that beaches with lower Dean values are beaches that are more ‘‘attractive’’ for tourist activities. Beaches in Bahía Coquimbo and Bahía La Herradura receive a high load of visitors in summer and are also subjected to mechanical cleaning and even sometimes the removal of algae stranded on the shore by the use of mechanical plows (Loyola, 2012). Both bays have shown massive tourism development during the last 10 years, with a high occupancy of the dunes for construction of different entertainment and accommodation services, whose impact on natural communities has not been evaluated. Although the impacts are not immediately visible, as explained by Schlacher and Thompson (2012), the ramifications of the impact that human activities can have on the macrobenthos are wide and can affect the functions of sandy beach ecosystems. In northern Chile, P. maculata is located in the high tide fringe, called the ‘‘drying zone’’, where it is accompanied by Excirolana braziliensis (Jaramillo et al., 1998); in the areas sampled in this study, we also found it sharing space with O. tuberculata. Although these two species of crustaceans have been described as the most abundant in the upper intertidal sandy Chilean coast, they are smaller in body size than P. maculata, such that their biomass can far exceed their contribution to organic matter in the beach ecosystem. P. maculata larvae can reach sizes close to 20 mm, and adults are approximately 10 mm in size; the average weight is approximately 0.05 g for the adult and approximately 0.02 g for larvae (Vega et al., 2007). Considering the average weight and density of Coleoptera recorded in this study, the biomass of P. maculata may reach high values, such as at Caleta Hornos, where the biomass would be estimated at 2 g m2. These values are significant for the highest fringe of the beach, where available organic matter is very low. P. maculata abundance in this study (max. approx. 50 individuals m2) reached higher values than recorded in other places, such as the beaches of Portugal (
