Main factors determining bioerosion patterns on rocky cliffs in a drowned valley estuary in the Colombian Pacific (Eastern Tropical Pacific)

Geomorphology 246 (2015) 220–231

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Main factors determining bioerosion patterns on rocky cliffs in a drowned valley estuary in the Colombian Pacific (Eastern Tropical Pacific) Alba Marina Cobo-Viveros ⁎, Jaime Ricardo Cantera-Kintz Department of Biology, Faculty of Natural and Exact Sciences, Universidad del Valle, Calle 13 #100-00, Cali AA. 25360, Colombia

a r t i c l e

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Article history: Received 6 August 2014 Received in revised form 8 May 2015 Accepted 10 May 2015 Available online 7 June 2015 Keywords: Bioerosion Grain size distribution of rocks Boring volume Rock porosity Bioeroding fauna Rocky cliffs Eastern Tropical Pacific

a b s t r a c t Bioerosion is an important process that destroys coastal rocks in the tropics. However, the rates at which this process occurs, the organisms involved, and the dynamics of rocky cliffs in tropical latitudes have been less studied than in temperate and subtropical latitudes. To contribute to the knowledge of the bioerosion process in rocky cliffs on the Pacific coast of Colombia (Eastern Tropical Pacific) we compared: 1) boring volume, 2) grain size distribution of the rocks, and 3) rock porosity, across three tidal zones of two cliffs with different wave exposure; these factors were related to the bioeroding community found. We observed that cliffs that were not exposed to wave action (IC, internal cliffs) exhibited high percentages of clays in their grain size composition, and a greater porosity (47.62%) and perforation (15.86%) than exposed cliffs (EC, external cliffs). However, IC also exhibited less diversity and abundance of bioeroding species (22 species and 314 individuals, respectively) compared to the values found in EC (41.11%, 14.34%, 32 and 491, respectively). The most abundant bioeroders were Petrolisthes zacae in IC and Pachygrapsus transversus in EC. Our findings show that the tidal zone is the common factor controlling bioerosion on both cliffs; in addition to the abundance of bioeroders on IC and the number of bioeroding species on EC. The integration of geology, sedimentology, and biology allows us to obtain a more comprehensive view of the patterns and trends in the process of bioerosion. © 2015 Elsevier B.V. All rights reserved.

1. Introduction Bioerosion is an important process that destroys coastal rocks in the tropics (Trenhaile, 1987); it occurs through the biological breakdown and removal of hard substrates by surface abrasion and boring. During surface abrasion, endolithic and grazing organisms (e.g., molluscs, echinoderms, fish, and some crustaceans) rasp, bite and scrape away a thin layer of rock (Trudgill, 1985; Trenhaile, 1987), produce particulate detritus (Torunski, 1979), and obtain nutrition from endolithic algae. During boring, perforating organisms (e.g., endolithic bacteria, algae, fungi, and lichens; sponges, sipunculans, polychaetes, bivalves, crustaceans, and echinoderms) directly remove rock material and weaken the remaining rock, making it more vulnerable to mechanical wave erosion and weathering (Trenhaile, 2005). As a consequence of these two processes, rocks collapse and decompose (Hutchings, 1986; Ricaurte

⁎ Corresponding author at: Instituto de Investigacións Mariñas, Rúa Eduardo Cabello 6, 36208 Vigo, Pontevedra, Spain. E-mail addresses: [email protected], [email protected] (A.M. Cobo-Viveros), [email protected] (J.R. Cantera-Kintz).

et al., 1995; Cantera et al., 1998), generating new substrates, changing cliff structure, and enriching the surrounding ecosystems with sediments and rocks from the fallen material, thus modifying the biological community. Not all marine organisms destroy the underlying rock; some can also protect it from incoming waves and physicochemical attack by forming organic crusts in the lower intertidal and upper subtidal zones (rhodophytes: Lithothanium, Lithophyllum; chlorophytes: Halimeda; sublittoral brown algae; barnacles: Chthamalus, Balanus; limpets: Patella, Lottia, Fissurella, Siphonaria, Crepidula) (Trenhaile, 1987). However, determining the scale used to identify the role played by organisms involved in bioerosion can be difficult (Fornós et al., 2006): sometimes it is clear that an individual acts as a bioeroder or as an occupant nestler of a previously existing hole (while modifying it), but this is not always easy to ascertain. For example: encrusting organisms that have an important role in protecting the rock surface from physical erosion (Focke, 1977) sometimes also act as bioeroders; they can take away some rock when removed from the cliff (e.g., barnacles), or they can weaken what they are supposedly protecting by chemical or other processes (e.g., micro and macroalgae) (Naylor and Viles, 2002). Cliffs are also destroyed by mechanical and chemical means (McLean, 1974). Wave erosion is considered the dominant mechanical erosional agent in many parts of the world (Trenhaile, 1987); it

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occurs through steady wave action, generation of high shock pressures (Trenhaile and Kanyaya, 2007; Bezerra et al., 2011), or the abrasion from sweeping, rolling, or dragging of rocks and sand (Trenhaile, 1987). Chemical weathering is the result of a series of chemical reactions (Trenhaile, 1987) that modify the rock carbonate chemical equilibrium when working together (Trudgill, 1985). Some conceptual models of erosion on rocky coasts highlight the importance of the wave force/rock resistance relationship and leave aside that of biological agents (Sunamura, 1994) but the effects of chemical, mechanical, and biological erosion can be synergistic (Hutchings, 1986). The reconceptualization of Naylor et al. (2012) demonstrated that most of the geomorphologic processes are affected by organisms and included biological agents as important reducers of the resisting force of the rock. There has been a growing interest in rock coast geomorphology in temperate and sub-tropical latitudes (Naylor et al., 2010), but bioerosion rates and dynamics of rocky cliffs in tropical latitudes have been less studied (Moses, 2013). Some publications integrate biological, geological and sedimentary variables (Fischer, 1981a,b; Cantera et al., 1998), and quantify cliff retreat (Ricaurte et al., 1995; Cantera et al., 1998) and bioerosion rates of several organisms (Rasmussen and Frankenberg, 1990; Toro-Farmer et al., 2004; Herrera-Escalante et al., 2005; Asgaard and Bromley, 2008; Lozano-Cortés et al., 2011). Cantera et al. (1998) measured erosion rates and studied the biodiversity, zonation, and types of cavities made by perforating fauna in two rocky cliffs in Buenaventura Bay (Pacific coast of Colombia). Additionally, there are some works that studied perforations by crustaceans and bivalves (Cantera and Blanco-Libreros, 1995; Ricaurte et al., 1995), and that quantified the erosion rate of sea urchins in rocky cliffs (Lozano-Cortés et al., 2011). However, little work has been done on bioerosion of rocky cliffs in Colombia, in spite of the impact it can have on nearby human settlements living on top of the cliffs or near them. This process requires further study (Correa and Gonzalez, 2000). The present study contributes to the knowledge of the grain size distribution and boring volumes of two rocky cliffs in a drowned valley estuary in the Colombian Pacific (Eastern Tropical Pacific). As intertidal bioerosion cannot be understood without biological processes (Trudgill, 1985), boring volumes are used as a quantitative bioerosion indicator relative to wave exposure, tidal zone, and the bioeroding community found. Combining the effects of several bioerosion variables can indicate the areas that erode more quickly, compared to studying the effects of each variable separately.

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2. Materials and methods 2.1. Study site Buenaventura Bay is an ancient drowned valley estuary located in the Pacific coast of Colombia, between 3°48′N–3°54′N and 77°05′W–77°20′W (Fig. 1). It is located in one of the most humid places of the world: the average annual precipitation rate is more than 7000 mm/year, which makes chemical erosion very high. Buenaventura Bay has a tropical hot and humid rainforest climate: the mean annual temperature is 26.2 °C, and the mean relative humidity is 89%. The rainy season occurs between August and November. Waves can reach heights of 2 m outside the bay, but they are rapidly reduced to 0.9 m near the entrance due to energy dissipation related to floor friction. The bay undergoes forcing by semi-diurnal tides with a meso-macrotidal range of 4 m (Cantera and Blanco, 2001). The north side of Buenaventura Bay is characterized by vertical to sub-vertical cliffs that range from 10 to 20 m in height, cut into horizontal to sub-horizontal Tertiary sandstones, shales and mudstones (Correa and Morton, 2010). The tops of the cliffs are covered with dense vegetation, as occurs in most humid tropical regions (Trenhaile, 1987). The cliffs located on this side of the bay are composed by the Raposo and Mayorquín geological formations (of sedimentary origin) from the Superior and Median Tertiary (Galvis and Mojica, 1993; Martínez, 1993); these formations consist of shale, mudstones, and dark gray siltstones organized in layers that vary from a few centimeters to 2 m thick. Coarse sediments (sandstone, slabs and clusters) are also present, randomly arranged between the strata (Cantera et al., 1998). Two cliffs located on this side of the bay were chosen (Fig. 1): one on the external zone (EC, located 0.5 km from the entrance and exposed to wave action) and the other on the internal zone (IC, located 15.4 km from the entrance of the bay and not exposed to substantial wave action). Sedimentary deposits of continental origin reach Buenaventura Bay through the rivers flowing into it; these sediments particularly affect cliffs in IC so that the rocks forming these cliffs are softer than the ones forming EC. 2.2. Sampling Nine blocks of approximately 15 cm × 15 cm × 15 cm were extracted from each cliff, using a chisel: three from the supralittoral,

Fig. 1. Geographical location of the cliffs studied. Right: South America, showing the location of the Pacific coast of Colombia (Middle). Left: Buenaventura Bay, showing the locations of IC (unexposed cliffs) and EC (exposed cliffs).

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three from the upper intertidal, and three from the lower intertidal. These three tidal zones were distinguished based on the characteristic algae, perforations, and tidal coverage: the high zone (Supralittoral or splash zone) is covered by patches of the algae Cladophora albida, Cladophora herpestica (or a mix of both), and Bostrychia tenella; it is poorly bored and is only covered by the tide during spring tides, but other than that it only receives the splash from waves that break in the inferior tidal levels. The upper intertidal zone (or Superior Mesolittoral) is covered by Bostrychia radicans, with patches of Cladophoropsis sp. and Boodleopsis verticillata; it is slightly perforated and it stays submerged for a longer period of time than the high zone. The lower intertidal zone (or Inferior Mesolittoral) can present coverage by B. radicans; it is the most perforated zone, it stays submerged for longer periods of time than the other two zones, and it is sometimes separated from the upper intertidal zone in this locality by a stratum of volcanic, hard rock covered by oysters and barnacles (see Fig. A1 in the Appendix). After the blocks were extracted from the cliffs, they were submerged in a mixture of water, alcohol, and clove oil in order to collect all the benthic fauna within the rock (which was preserved in 70% alcohol); partial desalinization occurred in this process. The fauna collected inside the blocks were identified using taxonomic keys for each group (Haig, 1960; Olsson, 1961; Keen, 1971; Fauchald, 1977; Brusca, 1980; Brusca and Iverson, 1985; Froidefond, 1985; Williams, 1986; Kim and Abele, 1988; Abele and Kim, 1989; Ríos and Ramos, 1990; Poore, 1994; Hilbig, 1997; Cantera et al., 1998). The organisms were marked and preserved in 80% alcohol. The blocks of rock were cored into smaller blocks of approximately 10 cm × 10 cm × 10 cm. To determine the perforation volume, the rocks were first saturated in water (submersion time depended on the characteristics of each block), taken out, and the liquid remaining inside the perforations was extracted. Afterwards, the rocks were weighed in air (with an electronic balance of precision ± 0.1 g) and in water (see Fig. A2 in the Appendix), calculating their volume from the weight difference in both environments. The volume of rock (VR), including perforation volume (due to bioerosion) and porosity volume (due to the incipient rock porosity), was found using Eq. (1):

V R ¼ WR −WsR =δwater

ð1Þ

where WR is the weight of rock + rock pores in the air, WsR is the weight of rock + rock pores in the water, and δwater is the water density. The volume of rock without perforations (VT) was found by filling the boreholes with modeling clay, sealing the rock with paraffin wax, weighing the block in air and water, and applying Eq. (2). V T ¼ W RC −W sRC =δwater

ð2Þ

WRC is the weight of the sealed rock in air, and WsRC is the weight of the sealed rock in water. The volume of rock due to perforations (VP) was calculated from the difference between VT and VR (Eq. (3)). VT ¼ VR þ VP

ð3Þ

2.3. Specific gravity The specific gravity (Gs) of any substance is the unitary weight of the material divided by the unitary weight of distilled water at 4 °C. This variable is used in the hydrometer analysis (Bowles, 1981a) to obtain the void ratio of a soil or ground, and to predict its unitary weight

(Eq. (4)). The methodology is described in Bowles (1981a). 
   Gs ¼ W sol = W sol − W f w −W f ws =δwater

ð4Þ

Wsol is the weight of the solids, Wfw is the weight of the flask + water, and Wfws is the weight of the flask + water + solids. 2.4. Hydrometer analysis This analysis estimates the particle size distribution of soils that contain a considerable amount of particles between 0.075 and 0.001 mm (clay and silt). The Stokes Law (Eq. (5)) estimates the falling rate of spheres in a fluid (v, in cm/s) from the specific weight of the spheres (γs = density × g = (mass/unit of volume) × gravity, in g/cm3), the specific weight of the fluid (γf, usually water), the absolute viscosity or fluid dynamic (η, in dynes × seg/cm2) and the sphere diameter (D, in cm) (Bowles, 1981a; Das, 2001).  v ¼ 2γ s −γ f =9η  ðD=2Þ2

ð5Þ

This equation is valid for particle diameters between 0.0002 and 0.2 mm. Temperature was taken into account, since the specific weight and viscosity of water depend on this variable. The hydrometer analysis was performed on the rocks from the cliffs and on a control solution prepared with 125 ml of 4% sodium hexametaphosphate (NaPO3, a dispersing agent which neutralizes the charges on the smallest grain sizes that often have negative charge) and sufficient distilled water to produce 1000 ml. The hydrometer was put into the control cylinder to record zero and meniscus corrections; the temperature was measured as well. To prepare the sample for the hydrometer analysis, the blocks of rock were crumbled and dried at 110 °C for 24 h, after which they were macerated and passed through the #200 sieve to obtain a 50 g sample (see Fig. A2 in the Appendix). 125 ml of 4% NaPO 3 were added to the sample and the resulting mixture was left standing for 24 h. Afterwards the mix was transferred to a dispersion (or malt mixer) cup and water was added until the cup was about twothirds full. The contents were mixed for a minute, and then the mixture was carefully transferred to a 1000 ml sedimentation cylinder. Any soil left in the dispersion cup was rinsed using a plastic squeeze bottle and the remains were poured into the sedimentation cylinder. Next, water was added until the 1000 ml level and the mixture was agitated again for 1 min to homogenize the material within the column; this was done by placing the palm of the hand over the open end and turning the cylinder upside down and back. Finally, the sedimentation cylinder was set on a table and a ASTM 152H hydrometer was inserted; readings were taken at the time intervals t = 0.5 min, 1 min, 1.5 min, 2 min, 2.5 min, 3 min, 3.5 min, 4 min, 8 min, 16 min, 30 min, 60 min, 120 min, and 240 min, or until the reading became constant. Readings were always taken at the upper level of the meniscus because suspended soil water solution makes the system opaque. Temperature was also recorded at each time interval. After all the readings were taken, a series of corrections were performed due to zero, meniscus and temperature (Bowles, 1981b). The zero correction (Cz) is applied to the actual hydrometer reading depending on the hydrometer's zero reading in the control cylinder: if this reading is below the water meniscus, Cz will be positive; if it is above, it will be negative; and if the reading is at the meniscus, Cz will be zero (Bowles, 1981a). The meniscus correction (C m ) is the difference between the upper level of meniscus and water level of the control cylinder (Bowles, 1981a). The temperature correction (CT) is done when the temperature of the soil suspension is not 20 °C (hydrometers are generally calibrated at this temperature); if it is

A.M. Cobo-Viveros, J.R. Cantera-Kintz / Geomorphology 246 (2015) 220–231 Table 1 Grain size composition (percentage) of unexposed (IC) and exposed cliffs (EC) in the Pacific coast of Colombia. Particle diameter Fine sands Silts Clays

b75 μm b50 μm b20 μm b10 μm b2 μm

EC

100% 80–92% 40–51% 11–30% 9–11%

100% 62–86% 28–45% 8–15% 0%

above, the hydrometer reading will be less and CT will be positive (and vice versa) (Bowles, 1981a). CT was determined from Table A1 in the Appendix. The corrected hydrometer reading (Rc) was calculated from the actual reading (Rreal) as follows: Rc ¼ Rreal −Cz þ CT :

ð6Þ

The percent finer (P, percentage of particles that go through the sieve) was calculated as follows P ¼ Rc  a  100=Ws

The equivalent particle diameter (D, in mm) was calculated using the following formula: D¼K

IC

ð7Þ

where “a” is a correction factor used whenever the Gs of soils is different from 2.65 (the Gs at which the 152H hydrometer was calibrated). It was determined from Table A2 in the Appendix using Gs. Ws is the weight of the soil sample (in g).

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pffiffiffiffiffiffiffi L=t

ð8Þ

where the factor K is a function of temperature, Gs and water viscosity; for the known Gs of the soil, K was obtained from Table A3 in the Appendix. L is the effective hydrometer depth L (in cm) obtained from Table A4 in the Appendix for the meniscus corrected reading; and t is the time interval (in min). Grain size distribution curves (D) were plotted versus the percent finer (P) on a semi-logarithmic plot. 2.5. Statistical analysis The percentage of perforation and porosity volumes were determined and compared between tidal zones of each cliff with a one-way ANOVA, and between both cliffs with a two-way ANOVA. Homogeneity of variances was tested for using Levene's test. Bioeroder abundance and number of bioeroding species between tidal zones was compared with a one-way ANOVA, and between cliffs with a two-way ANOVA, because normal distribution and homogeneity of variances are not critical to perform an ANOVA when sample sizes are equal (Hammer and Harper, 2008). If the ANOVA showed significant inequality of means, the post-hoc Tukey–Kramer pairwise comparison was used (Hammer et al., 2001). The percentage of biodegraded volume was related to the abundance and richness of eroding fauna, tidal zone, and percentage of

Fig. 2. Grain size distribution of A. unexposed (IC) and B. exposed cliffs (EC) on the Pacific coast of Colombia. The legend on the right represents each tidal zone: low (L), middle (M), and high (H).

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natural porosity of the rock using a simple correlation analysis (Zar, 2010). The correlation coefficients were compared with a one-way ANOVA. Finally, to determine if the combined effect of all factors on the bioerosion process was higher than the effect of each factor taken separately, a multiple regression analysis including perforated volume, richness and abundance of bioeroding fauna, tidal zone, and volume of natural porosity of the rock, was performed. 3. Results 3.1. Composition of cliff sediments Both cliffs are composed mainly of shale. In the hydrometer analysis, both cliffs showed a high percentage of fine particles in their grain size distribution, but unexposed cliffs (IC) showed finer particles than exposed cliffs (EC) (Table 1, Fig. 2A). In fact, we found particles smaller than 2 μm (clays) in IC but not in EC (Table 1, Fig. 2B). One curve from the low (L) and another from the middle (M) tidal zone in EC (blocks L1 and M1, Fig. 2B) differed from the rest of the cliff's grain size distribution. They represent an inclusion of hard rock that occurs along these kinds of cliffs, with a thicker composition than the rest of the analyzed samples: only 40% of the particles exhibited diameters b50 μm (silts) and 15–20% b 20 μm (silts). 3.2. Perforation and porosity volumes More perforation volume (produced by bioerosion of the rock) was found in the low and high tidal zones of IC, but the middle tidal zone was more densely perforated in EC (Table 2). Significant differences were found in the perforation volume between tidal zones in EC (p = 0.001) due to dissimilarities between the high and low (p = 0.004) and the high and middle tidal zones (p = 0.002). Significant differences were also found when we compared the perforation volume of both cliffs (p = 0.002), between the low tidal zone in IC and the high tidal zone in EC (p = 0.012), and between the high and middle tidal zones in EC (p = 0.017). Significant differences were not found in perforations between wave exposures (p = 0.666) or an interaction between wave exposure and tidal zones (p = 0.126). Significant differences in the porosity volume (incipient rock porosity) were found between wave exposures (p = 0.016) because IC showed more porosity than EC in all tidal zones; these differences were due to dissimilarities between the high tidal zone in IC and the low tidal zone in EC (p = 0.039). There were no significant differences in porosity between tidal zones (p = 0.146), nor an interaction between wave exposure and tidal zone (p = 0.336). Table 2 Percentage of perforations due to bioerosion (relative to total volume) and percentage of porosity (relative to volume of solids + volume of pores) found for the three tidal zones of unexposed cliffs (IC) and exposed cliffs (EC) in the Pacific coast of Colombia. Richness and abundance of bioeroding species of the studied cliffs is also shown. Cliffs

IC

EC

Perforations (%)

Porosity (%)

Abundance (individuals)

Richness (number of species)

Low Middle High Average

25.08 14.37 8.14 15.86

46.39 47.04 49.41 47.62

Total

183 99 32 314

18 13 11 22

Low Middle High Average

21.02 23.93 0.30 15.08

34.15 41.20 45.65 40.33

Total

295 123 73 491

25 14 4 32

Fig. 3. Abundance of bioeroding species in the low, middle and high tidal zones of A. unexposed cliffs (IC) and B. exposed cliffs (EC) in the Pacific coast of Colombia. The category “Others” groups bioeroding fauna with total abundances of less than 10 individuals.

3.3. Bioeroding fauna We found 314 individuals belonging to 22 macrobioeroding species in IC (Table 2). More bioeroder species and abundance of grazers and borers were found in the low tidal zone (58.3%). Petrolisthes zacae was the most abundant species in this cliff (41.1%; Fig. 3A) because it appeared in great numbers in the low and middle tidal zones. The amphipod Chelorchestia sp. was the most abundant in the high tidal zone (relative abundance of 37.5%). Significant differences were found in the abundance of bioeroders between the high and low tidal zones (p = 0.004) but not in the number of bioeroding species (p = 0.086). A total of 491 individuals belonging to 32 bioeroding species were found in EC, concentrated in the low zone (25 bioeroder species and 60% of total cliff abundance). Pachygrapsus transversus, Alpheus javieri and Upogebia tenuipollex were the most abundant species in this cliff (relative abundances of 18.1%, 14.5%, and 12.4%, respectively; Fig. 3B and Fig. A1 in the Appendix). However, Petrolisthes armatus, P. transversus and Ligia baudiniana were the most abundant for the low, middle, and high tidal zones (48, 38, and 59 individuals, respectively). Significant differences were found in the number of bioeroding species between the high and low tidal zones (p = 0.029), but not in the abundance of bioeroders (p = 0.104). When both cliffs were compared, significant differences were found in the abundance of bioeroders between the high zone in IC and the low zone in EC (p = 0.018). We also found significant

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Fig. 4. p-value, correlation (r) and determination coefficients (r2) found for significant linear correlations in unexposed cliffs (IC; A–B) and exposed cliffs (EC; C–D) on the Pacific coast of Colombia. Biodegraded volume was negatively correlated with tidal zone in both cliffs (A and C), and positively correlated with abundance of bioeroders in IC (B) and with richness of bioeroders in EC (D).

differences in the number of species between the low and high tidal zones in EC (p = 0.011). However, there were no significant differences in the abundance or richness of bioeroders between wave exposures (p = 0.149 and p = 0.876, respectively), nor in the interaction between wave exposure and tidal zone (p = 0.621 and p = 282, respectively).

3.4. Relationship between cliff composition and bioeroding fauna The perforation volume in both cliffs was negatively correlated to tidal zone (IC: r = − 0.686, p = 0.041, Fig. 4A; EC: r = − 0.782, p = 0.022, Fig. 4C) but positively correlated with the abundance of

Table 3 Multiple regression analysis comparing volumes of perforation with tidal zone, volume of natural porosity of the rocks, richness and abundance of bioeroding fauna in unexposed (IC) and exposed cliffs (EC). Multiple correlation coefficient (R), multiple determination coefficient (R2), and adjusted coefficient of determination are shown (R2a ), as well as results of ANOVA for the multiple regression data. Statistics Multiple R Multiple R2 Adjusted R2a F p

IC

EC

0.797 0.635 0.271 F(4, 4, 0.95) = 1.746 0.301

0.916 0.839 0.625 F(4, 3, 0.95) = 3.922 0.145

bioeroders in IC (r = 0.74, p = 0.023, Fig. 4B), and with the richness of bioeroders in EC (r = 0.725 p = 0.042, Fig. 4D). The combination of factors did not indicate a statistically significant effect on the percentage of perforations found for any of the cliffs. However, the R2 values indicate that 63.5% (83.9%) of the total variation of perforations in IC (EC) is explained by the regression (Table 3). R2 values are higher in EC than in IC, indicating that all variables chosen for the analysis influence the percentage of perforations found in EC, but not in IC. 4. Discussion 4.1. Sediment composition of the cliffs Our findings confirm the fine sediment composition of the rocks forming the cliffs on the Pacific coast of Colombia, which is mainly due to differences in particle sedimentation rates during cliff formation, and to the energy of the deposition environment. The sedimentary rocks forming the cliffs are composed of ancient mud and silt and were produced by accumulation of sediments from the river flow. Unexposed cliffs (IC) were formed by sediments from rivers flowing into Buenaventura Bay, which is why they have clays only in the higher and middle zones and few hard substrata inclusions (as seen by the higher percentage of small grain sizes). The presence of coarse particles in the rocks between layers of fine sediments in the low and middle tidal zones of exposed cliffs (EC; blocks L1 and M1 in Fig. 3B) is due to the Raposo Mayorquín formation, characterized by the presence of coarse sediments (sandstone, slabs and clusters) randomly arranged

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between the strata (Cantera et al., 1998). These coarse sediments result from the consolidation of sediments from the river flow that subsequently changed the grain size composition of the original Mayorquín formation. It is important to recognize that different agents of bioerosion may operate in distinct zones across shore platforms (Naylor et al., 2012): for example, biological weathering and erosion-enhancing agents are typically found in morphologically lower, moister positions of shore platforms (our lower intertidal zones) (Naylor et al., 2012), whereas chemical/physical weathering agents are likely to be relatively more important in drier, morphologically high points where wetting/drying and swelling/contraction are more common (our supratidal zones) (Gómez-Pujol and Fornós, 2009). Wave action is weaker in the tropics than in high latitudes, and younger limestones or shales are physically much weaker (Trenhaile, 1987). EC receives a more constant and higher wave action than IC, which can affect its porosity by removing smaller particles from the cliff in the first stages of erosion, causing abrasion on the bigger particles that are left. However, even though EC is more exposed to waves and we expected this cliff to be more perforated, it seems that porosity volumes play a more important role in determining perforation volumes. Trudgill (1985) established that increased porosity decreases rock resistance to erosion compared to that of well-cemented rocks with few joints; so the increased porosity in IC makes this cliff more susceptible to erosion, in spite of it being less exposed to waves. In addition, although waves perform the erosive work, it is the tidally modulated distribution of wave energy that determines where this work is performed (Trenhaile, 1978). The lower tidal zones of both cliffs stay submerged longer than the other zones as a result of the semi-diurnal tidal cycle of Buenaventura Bay; this benefits the bioerosion community inhabiting the lower zones of both cliffs, enhancing the higher perforation volume exhibited by them. Bioerosion (in some cases) is greatest in sheltered sites because wave shock and mobile sedimentary particles driven by waves and currents can prevent colonization of exposed areas by some organisms (Trenhaile, 1987). Cliffs in IC are exposed to higher river discharges and a low wave impact; this allows a “film” to be formed on the surface of these cliffs, protecting them from rain and growth of microbioeroders (e.g., algae). Hutchings et al. (2005) found a similar effect on coral bioerosion. In cliffs in IC, this film also hinders grazer colonization and increases the presence of bioeroding larvae in all tidal zones in IC that otherwise would be eaten by grazers feeding on the algae. 4.2. Bioeroding fauna The difference in species richness between tidal heights of the cliffs is that exposed sites (as EC) have better humidity and shelter conditions that allow higher species richness in the lower tidal zones, especially of the representative species (P. armatus, A. javieri, U. tenuipollex). On the other hand, species typical of the high tidal zone (Chelorchestia sp., P. zacae, P. transversus) dominate sheltered sites (as IC) (Palmer et al., 2003). The boring habit is well developed in four pelecypod families: Pholadidae and Petricolidae (mainly mechanical borers) and Gastrochaenidae and Mytilidae (largely chemical borers that require a calcareous substrate) (Yonge, 1955; Trenhaile, 1987). Drilling Mytilidae species have been reported as responsible for the greatest amount of perforations in hard rocks (Cantera et al., 1998), while species of Petricolidae (Ansell, 1970) and Pholadidae have been for soft rocks (Warme and Marshall, 1969; Pinn et al., 2005, 2008). In this study, we found Cyrtopleura crucigera (Pholadidae) in both cliffs, while Sphenia fragilis (Myidae) and Pholadidea tubifera (Pholadidea) were found in EC only (see Fig. A1 in the Appendix). These findings differ from results previously found for the area, where C. crucigera, S. fragilis and Pholadidea sp. 1 were

found in IC (Cantera et al., 1998). Three species of bivalves were found in EC that were reported as borers by Keen (1971): Cryptomya californica (Myidae), Ensitellops hertleini (Basterotiidae), and Barnea subtruncata (Pholadidae). The mytilid species Brachidontes playasensis was found in low abundances in the low zone of cliffs in IC, where it could be playing an important role in protecting the rock surface from physical erosion. Crustaceans, on the other hand, have been reported as borers of wood (Davidson and de Rivera, 2012), sandstones (Cadée et al., 2001), and basalts (Fischer, 1981b). U. tenuipollex and A. javieri are boring decapods in cliffs of the Colombian Pacific coast (Ricaurte et al., 1995). They were found in great numbers in EC but not in IC, where they were outnumbered by Alpheus villus, Upogebia spinigera, and Upogebia burkenroadi. These three species may be taking an active part in the bioerosion process in cliffs that are less exposed to wave action. Several worms are also active borers in calcareous and noncalcareous substrates (Trenhaile, 1987). Hutchings and PeyrotClausade (2002) recognize polychaetes and sipunculans as dominant groups of macro-boring organisms in newly available dead coral substrate, facilitating the subsequent recruitment of other boring organisms such as sponges and bivalves. For the Pacific coast of Colombia, Cantera et al. (1998) found Polydora sp. in cliffs in EC. However, although we found three species of polychaetes inhabiting the rock burrows in EC (Nereis sp., Lysidice sp. and Syllis sp.) and two in IC (Nereis sp. and Neanthes sp.), we did not find Polydora within our samples. Of the genera found, Lysidice has been found to be burrowing inside Porites colonies (Hutchings, 2008), so they could also be boring into rocky cliffs. We only found one individual of the sipunculid genus Phascolosoma in a rock burrow in the lower tidal zone of EC (data not shown), contrary to previous findings that highlighted their importance on the bioerosion process in cliffs of the Pacific coast of Colombia (Cantera et al., 1998). Our evidence indicates that molluscs and crustaceans are more important than polychaetes and sipunculans in the bioerosion process in the cliffs that were studied.

4.3. Contribution of bioeroding fauna to perforation volumes Previous authors found that a greater biological contribution to erosion rates occurs on sheltered shores compared to exposed ones (Trudgill, 1976; Spencer and Viles, 2002; Moura et al., 2012). This coincides with our findings, in which IC presented better conditions for the establishment of bioeroder communities, which in turn was reflected in a higher volume of perforation found compared to EC. Naylor et al. (2012) highlighted the importance of the biological role in the removal of rocky masses and the erosion of rocky coasts (which had been previously neglected). The direct erosional role of grazing organisms is of particular significance on tropical and warm temperate limestone coasts, where wave attack may be fairly weak (Trenhaile, 1987). Grazing organisms always contribute directly to the erosion of rock surfaces, and their presence in IC can explain the higher porosity found here, despite the high percentage of small particle composition; macro- and micro-grazers facilitate the penetration of microflora into the substrate and indirectly weaken and increase rock porosity (Trenhaile, 1987; Naylor et al., 2012). Rock borers play a direct and indirect role in the disintegration of rocky substrates, particularly in the lower portions of the intertidal zone. Boring directly removes some rock material, but the rest is left susceptible to breakdown by wave action and other destructive mechanisms (Trenhaile, 1987). Borers also enhance the rock environment for algal colonization, and increase the area of rock surface exposed to other physical and chemical processes (McLean, 1974). The indirect role of rock borers may be of greater significance to the destruction of coastal rocks than the direct removal of material.

A.M. Cobo-Viveros, J.R. Cantera-Kintz / Geomorphology 246 (2015) 220–231

4.4. Bioerosion and habitat heterogeneity The higher number of perforations (providing refuge) and the time a cliff's tidal zone remains submerged, determined the higher richness and abundance of bioeroders inhabiting the burrows of the cliff's lower tidal zones. The tide determines how long a substrate is underwater or exposed (subject to desiccation) (Trenhaile, 1987), which partly depends on the tides being diurnal, semi-diurnal, or mixed (Johnson and Sparrow, 1961). This permits less desiccation, and changes in temperature and salinity (Palmer et al., 2003) in the cliff's lower zones. Biodiversity, in terms of number of species, is higher when suitable microhabitats for vagile species are present in addition to those available for sessile species. Bivalve and crustacean burrows provide more shelter for vagile species than irregularities in the naturally occurring substratum (such as crevices), and thus enhance the abundance and diversity of intertidal species low on the shore (Pinn et al., 2008). The use of crevices as shelter was seen in both cliffs by the presence of eight species of fish during low tide: Pisodonophis daspilotus, Cerdale ionthas, Gobulus hancocki and Erotelis armiger in IC; and Clarkichthys bilineatus, Cerdale paludicola, Microdesmus dipus and Pythonichthys asodes in EC. The fact that both cliffs are located near mangrove zones, which are known to act as nurseries, explains why Grapsidae, Porcellanidae and Ocypodidae crustacean megalops were found in these sites. 4.5. Further studies on tropical rocky cliffs Sea cliff erosion in the tropics is an understudied subject and there is a dearth of information on erosion rates and dynamics. Although it is a difficult task, the understanding of the relative contribution of wave impact and abrasion to total erosion rates through field measurements requires further study (Moses, 2013). Furthermore, the effects of climate change on erosion rates need to be more thoroughly studied, because the predicted increase of storm activity and/or intensity, sea-level rise and the interaction of both could contribute significantly to erosion (Phillips and Jones, 2006). To assess and predict the impacts of climate change, the understanding of bioerosion dynamics needs to be expanded to harder igneous and sedimentary rocks because studies have been largely limited to recent and relatively weak beach rock and reef limestone (Moses, 2013; Moses et al., 2014). Another item that could have important consequences — particularly for rocky cliffs in the Colombian Pacific — is the modification of seawater chemistry by organisms inhabiting the burrows. pH reduction during night hours (as an imbalance between photosynthesis during the day and respiration during the night) would increase the solubility of calcium carbonate in the rocks and facilitate their degradation. This process needs to be further studied.

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We suggest that the importance of crustaceans in the bioerosion process needs to be highlighted because it has always been given a secondary role. In addition to A. javieri and U. tenuipollex (previously reported as borers of the cliffs on the Colombian Pacific coast), we recommend that A. villus, U. spinigera and U. burkenroadi should be considered as active boring species in cliffs of IC. We also include C. californica, E. hertleini, and B. subtruncata as active borers for cliffs in EC.

Acknowledgments This project was supported and funded by the Universidad del Valle, Biology Department, Marine Biology Section, and by internal funding of the Research Vicerectory of the Universidad del Valle (CI 7980). We thank Philip A. Silverstone-Sopkin and Amparo Viveros for correcting the manuscript, Humberto Maya from the Biological Station of Universidad del Valle in Buenaventura, M. Cuellar, S. Cobo-Viveros, A.I. Vásquez, V. Izquierdo, F. Vejarano and the locals from Piangüita who helped during different times on the extraction of blocks from the cliffs. Biologists J.F. Lazarus, L.A. López de Mesa, E. Rubio, and L. Herrera from “Ecomanglares” research group, and B. Valencia helped during the flora and fauna identification process. C. Manrique and N. Durán from the Civil Engineering School at Universidad del Valle helped on the sedimentology processing of the rocks. E. Londoño was very helpful on statistical inquiries. Finally, thanks to R. Neira who helped in the organization of field trips and experimental design.

Table A1 Temperature correction factor (CT) applied to the actual hydrometer readings. Source: Bowles (1981a). Temperature (°C)

CT

15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30

−1.10 −0.90 −0.70 −0.50 −0.30 0.00 +0.20 +0.40 +0.70 +1.00 +1.30 +1.65 +2.00 +2.50 +3.05 +3.80

5. Conclusions Bioerosion is a process in which biological, geological, and geomorphological factors interact. For the Pacific coast of Colombia, the abundance of bioeroders (biological factor) and tidal zone (physical factor) were the most influential eroding factors on cliffs sheltered from wave action. On the other hand, tidal zone and richness of bioeroders (also a biological factor) were the most important in determining erosive volumes in cliffs exposed to wave action. Rock composition in IC presented smaller grain sizes than EC, resulting in more porous and perforated rocks. The highest abundance of bioeroding organisms was found in the lower tidal zones of both cliffs because this zone stays under water for a longer period of time, providing vital conditions for the fauna that takes refuge inside the cliffs during low tide. Boring bivalves were less abundant in this study compared to that of boring crustaceans.

Table A2 Correction factor “a” determined for unit weight of solids (specific gravity). Source: Bowles (1981a). Unitary weight soil solids (g/cm3)

Correction factor “a”

2.85 2.80 2.75 2.70 2.65 2.60 2.55 2.50

0.96 0.97 0.98 0.99 1.00 1.01 1.02 1.04

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Table A3 Values of K used in Eq. (7) for several combinations of unitary weights and temperatures to compute the particle diameter in the hydrometer analysis. Source: Bowles (1981a). Temperature (°C)

16 17 18 19 20 21 22 23 24 25 26 27 28 29 30

Gs 2.45

2.50

2.55

2.60

2.65

2.70

2.75

2.80

2.85

0.01510 0.01511 0.01492 0.01474 0.01456 0.01438 0.01421 0.01404 0.01388 0.01372 0.01357 0.01342 0.01327 0.01312 0.01298

0.01505 0.01490 0.01470 0.01450 0.01430 0.01410 0.01400 0.01380 0.01370 0.01350 0.01330 0.01320 0.01300 0.01290 0.01280

0.01481 0.01460 0.01440 0.01430 0.01410 0.01390 0.01370 0.01360 0.01340 0.01330 0.01310 0.01300 0.01280 0.01270 0.01260

0.01457 0.01440 0.01420 0.01400 0.01390 0.01370 0.01350 0.01340 0.01320 0.01310 0.01290 0.01280 0.01260 0.01250 0.01240

0.01435 0.01420 0.01400 0.01380 0.01370 0.01350 0.01330 0.01320 0.01300 0.01290 0.01270 0.01260 0.01240 0.01230 0.01220

0.01414 0.01400 0.01380 0.01360 0.01340 0.01330 0.01310 0.01300 0.01280 0.01270 0.01250 0.01240 0.01230 0.01210 0.01200

0.03940 0.01380 0.01360 0.01360 0.01330 0.01310 0.01290 0.01280 0.01260 0.01250 0.01240 0.01220 0.01210 0.01200 0.01180

0.01374 0.01360 0.01340 0.01340 0.01310 0.01290 0.01280 0.01260 0.01250 0.01230 0.01220 0.01200 0.01190 0.01180 0.01170

0.01356 0.01338 0.01321 0.01305 0.01289 0.01273 0.01258 0.01243 0.01229 0.01215 0.01201 0.01188 0.01175 0.01162 0.01149

Table A4 Values of L (effective hydrometer depth, in cm) for use in Stokes' formula to determine particle diameters using an ATSM 152H hydrometer. Source: Bowles (1981a). Original hydrometer reading (only corrected for meniscus) 0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30

Effective depth L (cm) 16.3 16.1 16.0 15.8 15.6 15.5 15.3 15.2 15.0 14.8 14.7 14.5 14.3 14.2 14.0 13.8 13.7 13.5 13.6 13.2 13.0 12.9 12.7 12.5 12.4 12.2 12.0 11.9 11.7 11.5 11.4

Original hydrometer reading (only corrected for meniscus) 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Effective depth L (cm) 11.2 11.1 10.9 10.7 10.6 10.4 10.2 10.1 9.9 9.7 9.6 9.4 9.2 9.1 8.9 8.8 8.6 8.4 8.3 8.1 7.9 7.8 7.6 7.4 7.3 7.1 7.0 6.8 6.6 6.5

A.M. Cobo-Viveros, J.R. Cantera-Kintz / Geomorphology 246 (2015) 220–231

229

Fig. A1. Bioerosive species of rocky cliffs in the Colombian Pacific coast. A. Grapsus grapsus. B. Boring Pholadidea sp. C. Fall and disintegration of rocks. D. Alpheus javieri. E. Eurypanopeus transversus. F. Pachygrapsus transversus. G. Upogebia sp. H. Eriphia squamata. I. Cliff zonation. J. Alpheus. villus. K. Cirolanid isopod. L. Upogebia sp. next to a Y-shaped perforation. M. Barnea subtruncata. N. Sphenia fragilis. O. Ligia baudiniana. P. Petrolisthes armatus.

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Appendix

Fig. A2. Blocks from the low (a), middle (b) and high (c) zones of both cliffs were first cubed and then weighted in air (d) and in water (e). Later on, perforations were filled with modeling clay (f) and sealed with paraffin wax (h, i). For the hydrometer analysis, the rocks were grinded and mixed with sodium hexametaphosphate and water (g). The materials used in the hydrometer analysis (j) also included, from left to right, an electronic balance, beaker, mortar, test tube of 1000 ml, sieve of #200, hydrometer, chronometer, sodium hexametaphosphate and thermometer.

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