INTRODUCTION

Bioerosion has been defined as organic erosive activity, i.e. the process of breakdown and/or modification of substrata by macro- and micro-organisms (Davidson et al., 2018; Viles, 2013). Bioerosion involves organisms scraping, grazing, boring, burrowing, or dissolving on and in substrata of varying hardness and composition in a range of environments (Kázmér and Taborosi, 2012). Boring oganisms perforate and remove consolidated rocks, whereas burrowers tunnel and displace loose unconsolidated materials. In coastal intertidal regions, common macrobioeroders include molluscs (especially bivalves, gastropods, and chitons), urchins, sponges, worms, and arthropods (crabs and isopods) (Davidson et al., 2018; Donn and Boardman, 1988; Kázmér and Taborosi, 2012). Bioerosion can have a profound effect on intertidal ecology as it modifies local environmental conditions at a small scale within the affected habitat. Bioerosion is also a significant geomorphological process leading to rock removal and sediment production, with the potential to modify other dynamic erosive processes (Wilson, 2013). In the intertidal and shallow marine habitats, isopods may burrow into sand, inhabit macroalgae, or bore into mangrove roots or other substrates (Arrontes, 1990; Davidson and de Rivera, 2010; De Ruyck, McLachlan, and Donn, 1991; Miranda and Thiel, 2008). Their reported boring activity is briefly reviewed here, and their potential to cause bioerosion, in the case of boring into rocks, is of specific interest.

A number of Sphaeromatid isopods have been reported to burrow or bore into various substrates and a number of locations worldwide, as listed in Table 1. Wood boring is reported among isopods of the Sphaeromatidae and Limnoriidae families (Cragg, Pitman, and Henderson, 1999; Harrison and Holdich, 1984) including in SE Asia and Borneo (Hossain and Bamber, 2013; Singh and Sasekumar, 1994). Several species of Sphaeroma are reported to bore into mangrove roots as well as manmade coastal wooden structures such as jetties. A number of studies have been conducted to document wood-boring species; the types of timber most frequently damaged; and possible measures to prevent damage to jetties, wharves, piers, and other marine structures (Cragg, 1988; Cragg, Pitman, and Henderson, 1999; Nair, 1984; Roszaini and Salmiah, 2015). Sphaeromatid isopods are also reported to damage polystyrene floats used in docks and marinas in several countries, including native species (e.g., in Indo and West Pacific) and non-native (i.e. introduced) species (particularly along the Pacific coast of North America) (Carlton and Iverson, 1981; Davidson, 2012). Not only do they do extensive damage to manmade structures, but they also produce microplastic waste (Davidson, 2012).

Table 1

List of isopods species of the genus Sphaeroma reported boring in wood, polystyrene, and rock substrates worldwide, as well as other reports for S. triste (unspecified whether boring or not).

In comparison to wood boring, rock boring is reported in less detail and in fewer studies (Table 1). Warme and Marshall (1969, p. 773), quoting Barrows (1919), stated that isopods such as Sphaeroma “can erode rocks with its mandibles.” Dharmaraj and Nair (1982) report destruction of laterite and hard clay embankments attributable to boring by Sphaeroma sp. along backwaters of the Indian SW coast. Sphaeroma sieboldii has been reported as actively boring stones and living in the holes in coast of Korea (Kim and Kwon, 1985). Davidson, de Rivera, and Carlton (2013, p. 116) mention isopods burrowing in “friable rock,” and Sphaeroma quoianum is reported to accelerate erosion in salt marshes because of prodigious burrowing by dense populations in mud, clay, and peat in the Pacific coast of North America (Davidson and de Rivera, 2010, 2012). This leads to erosion rates that are ∼300% higher in infested areas compared with noninfested ones. Sphaeroma triste Heller (1865) is reported to burrow into “porous clay” exposed on beaches in Indonesia (Sidabalok, 2013, p. 53), but no description of the bioerosive activity is given. In Iraq, Sphaeroma annandalei is reported to create networks of burrows in a variety of materials, including friable rock (Mohammad, 2014). Sphaeroma walkeri is generally “not considered to be a wood-boring species,” and it was suggested that the morphology of its mouthparts is “unlike that of the true wood-boring sphaeromatids” (Carlton and Iverson, 1981, p. 35, 41). The species has been reported to be found in holes and crevices, in empty barnacle shells and sponge canals, and under stones (Carlton and Iverson, 1981; Khalaji-Pirbalouty and Wägele, 2010). Khalaji-Pirbalouty and Wägele (2010, p. 9), however, report it to be a wood borer and that “it also burrows in to soft rock” in the Persian Gulf. Sphaeroma wadai is reported boring in intertidal sandstone in Japan; their population structure and reproductive biology have been studied in detail and related to the boring habit (Murata and Wada, 2002). These various references clearly indicate that although several Sphaeromatid species are capable of boring into soft rock substrates and that this behavior may be more widespread than currently reported, research on the bioerosive effect of species other than S. quoianum is generally lacking.

The potential bioerosive effect of several Sphaeromatid species, including S. triste, has not been previously described or studied in any detail, and previous research in the SE Asian region focuses on wood boring not rock boring. The aim of this research was to identify if and where bioerosion is occurring in the study area and to establish the identity of the species responsible. In addition, the goal was to study the morphology of the borings and their distribution and density in the rocky substrate as well as their relationship to other types of coastal erosion features described previously (Dodge-Wan and Nagarajan, 2019) to establish the potential for bioerosive effect of isopod boring. This study presents the results of initial and mainly qualitative surveys of bioerosion by isopods in sedimentary rocks outcropping within a 40-km-long stretch of the coastal region to the SW of Miri in Northern Sarawak, East Malaysia. Other forms of erosion attributable to nonbiological processes have also been researched and are described elsewhere (Dodge-Wan and Nagarajan, 2019).

METHODS

The methods include geological and biological field observations, photography, and measurement with limited sampling and laboratory analysis.

Perforations in rocks in the intertidal zone of the study area were initially noticed and photographed by the authors in 2007. Then, as part of this research, rock surfaces, and driftwood found in the intertidal zone along a 40-km stretch of coast were examined several times during low tide between June 2016 and February 2019. Surveys of cliff and wave-cut marine notch profiles were performed using tripod mounted Leica Disto D810 range meter. Survey data was plotted using AutoCAD 2014 software (Autodesk, Inc., 2019). Elevations were compared to water levels at the date and time of each survey with corresponding tide chart levels and are reported in meters above datum (mAD) with reference to Miri tide datum. Perforation density per area of rock surface was based on initial estimation in field and then measured from calibrated photographs and is described as follows: moderate (10 to 100 perforations per 100 cm²), high (100–500 perforations per 100 cm²), and very high (>500 perforations per 100 cm²). Within areas of high to very high clustered abundance of perforations, 43 rock surfaces were selected and photographed with scale. The density of perforations on rock surfaces was analysed using calibrated field photographs of 5 cm × 5 cm areas, and measurements were made from all or selected parts of the photographs, as described in the text, using AutoCAD 2014 software. In addition, to establish the maximum crowding, ten areas of 1 cm² were selected from within photos of the highest density zones for further analysis. Within these 1 cm² areas, perforations were counted on the photos, and the percentage of perforated area was measured. Casts of rock surfaces with isopod perforations were made in the field on areas that appeared to be abandoned by the live isopods, such as loose boulders. Casts were made using Hardex Clear Silicone Rubber sealant RS-850 by applying approximately 10 g to the rock surface and gently pressing to inject the sealant into the perforations. Casts were used to describe perforation shape, not for quantitative measurements. Small samples of rock and wood were removed, stored in ethanol, and examined in the laboratory under binocular microscope. In addition, a small number of specimens were extracted and preserved in 70% ethanol. It is likely that isopod sampling was biased toward larger adult individuals, which are easier to collect in the field. Isopod specimens were examined using a Nikon SMZ74 stereomicroscope equipped with auxiliary 2× G-AL objective. Measurement of isopod length from anterior tip of cephalon to posterior tip of pleotelson was made dorsally using microscope crosshair graduation and micrometer scale after gently depressing the specimens to lay them flat. Width was measured at the widest part of the body. The measurement unit of variation is given in standard deviation (±). Specimens were dissected under stereomicroscope, and elements were placed on microscope slides in glycerin for examination using a Nikon Eclipse LV100NPOL polarizing/reflecting microscope equipped with a Nikon DSF12 camera. Fragile perforated rock samples were soaked in ethanol and dried and coated in blue-stained Ranger Industries liquid Ice Resin. After resin curing, rock samples were cut with rock saw for microscope examination and thin section preparation. Thin sections were polished to approximately 30-micron thickness with carborundum grit and examined using a Nikon Eclipse microscope. Measurement of perforation size (n=35) and photography was performed under microscope using software NIS Elements Version 4.40 (Nikon, 2019). Isopod identification was based on the key provided by Harrison and Holdich (1984) in their worldwide review. Morphology and taxonomy are discussed briefly in the “Results” and in greater detail in Supplemental Material ( Section 4 (238_coas-36-04-03_s01.docx)).

General Characteristics of Study Area

The study area is a 40-km stretch of coast located south of the Baram and Miri River mouths and the city of Miri, in northern Sarawak (Figure 1). The coastline predominantly comprises sandy beaches with some isolated rock headlands. It trends NE-SW approximately parallel to the strike of the outcropping interbedded sandstones and mudstones. The rocks belong to the Miri and Lambir formations of Miocene age. The strata are tilted with dips ranging from 20° to subvertical. Numerous and varied erosional features occur in this dynamic coastline. The typology of erosion features in the rocky sections has been described by Dodge-Wan and Nagarajan (2019). The features range from macroscale erosion (mass wasting, rock falls, sea caves, and arches) to mesoscale features (widened joints and bedding planes, pockets, gullies, and runnels) (Dodge-Wan and Nagarajan, 2019). The isopod perforations described here are the most obvious microscale erosional feature.

Figure 1

Map of north Sarawak (East Malaysia) showing coastline and location of sites with sandstone outcrops in intertidal zone where isopod bioerosion was observed (black stars). Distance from Taman Selera to Tusan Beach is 32 km.

Within this area, sedimentary rocks were found outcropping in the intertidal zone at and around four specific sites, described here below in order from NE to SW (Table 2). Taman Selera is a long, narrow sandy beach adjacent to a rocky headland consisting of massive sandstones with wave cut notch and intertidal platform. Tusan and Peliau beaches are backed by tilted interbedded sandstone and mudstone cliffs with shallow wave cut notch and sea caves. Bungai beach comprises two bays with corrugated sandstone and mudstone surfaces exposed at low tide. Further details of the sites are given in the Supplemental Material ( Section 2 (238_coas-36-04-03_s01.docx)). At all sites, variable amounts of driftwood and anthropogenic debris (jetsam) occur, depending on tidal conditions and daily and seasonal weather conditions (monsoon). The climate is tropical with annual average rainfall of approximately 2700 mm (Dodge-Wan and Nagarajan, 2019). The tidal range is approximately 1.9 m (i.e. microtidal) and mixed, with a dominance of diurnal (Lim and Kho, 2010). Spring tide elevations range from 2.0 mAD (high) to 0.1 mAD (low), whereas neap tides range from 1.3 mAD (high) to 0.9 mAD (low). As a result of the tidal pattern, the intertidal zone may be periodically exposed to harsh sun when low tide occurs during daytime. Salinity varies from 21 to 30 ppt (Anandkumar, 2016) because of influence of freshwater through streams and rivers (Baram, Miri, and Sibuti rivers). At Tusan, a major stream occurs close to the site, which might explain the slightly lower salinity values. At Taman Selera and at Tusan beach, a film of freshwater may flow on the exposed rock surface above the intertidal zone after heavy rain.

Table 2

Locations where rock-boring isopods were observed along the coast of Sarawak (East Malaysia) from Miri (in NE) to Bungai beach (in SW).

RESULTS

Along the coastline between Miri and Bungai beaches, where interbedded sequences of relatively soft sandstones, siltstones, and mudstones are exposed in the intertidal zone, significant but localized areas of high and moderately dense isopod perforations on the rock surfaces are common. Hence, the phenomenon is not rare along this coastline. The isopod populations appear to be widespread and well established in this habitat. They have been present at the Tusan site since at least 2007 and perhaps much longer.

Distribution within Intertidal Habitat

Within the intertidal zone, isopod perforations are observed in the upper half of the intertidal zone. It should be noted that the lower half of the intertidal zone is generally covered with sand (below 1 mAD). The highest isopod perforations are found in the splash and spray zone up to 1 m above spring high tide level. Within the splash zone, isopod perforations are present but are quite rare and appear to be uninhabited (abandoned). The zone in which isopod perforations are most abundant—and the live animals are found—has a vertical extent of approximately 1 m ranging from around 1.6 mAD (i.e. 30 cm above neap high tide) to the top of the beach sand, which is at 0.5 to 1.2 mAD. In addition to isopods, the organisms observed within the intertidal zone include barnacles, small turban shaped gastropods (<1 cm long), sea slaters, rare oysters, small mussels, hermit crabs, microalgae, and fine green filamentous algae (Figure 2A). Barnacles and gastropods are common and locally clustered on rock surfaces. However, the surfaces that are intensely perforated with live isopods inside the borings are generally devoid of other macrofauna. Barnacles are common on erosion-resistant, hard, iron-rich crusts that are not colonized by isopods (Figure 3). Isopod borings that are unoccupied, i.e. abandoned, may subsequently be colonized by algae growth, barnacles, bryozoans, and gastropods.

Figure 2

Dipping rock strata with shallow wave cut notch in the intertidal zone at Tusan (A) and Peliau (B), showing typical enhanced erosion due to clustering of abundant isopod perforations. Particularly high density of isopod perforations is noted in rock surface concavities as well as on the joint faces (as on subvertical joint towards middle of photo A) and on fallen blocks (as in foreground photo B). Ruler is 1-m long. Strata dip angle is approximately 42° in (A) (Tusan) and 82° in (B) (Peliau). Photos taken on 12 and 13 July 2018 at spring low tide.

Figure 3

Detail of rock surface with iron-rich crust showing high density of isopod perforations in soft sandstone below the crust and numerous barnacles encrusting on the harder crust surface above. Photo 17 November 2007 Tusan site. Note: The Sphaeroma triste isopods are visible in many of the perforations in lower half of photo (e.g., at the arrow). The perforated rock has been further eroded, and some former cylindrical perforations have been reduced to their hemispherical blind ends (e.g., at circle), whereas others show erosion of the lateral walls (e.g., at rectangle). Scale bar is 1cm.

Three species of isopod were identified within the study area. They are S. triste (Heller, 1865), Dynamenella trachydermata (Harrison and Holdich, 1984), and Iais singaporensis (Menzies and Barnard, 1951). It is possible that further investigation would reveal additional isopod species in the intertidal zone. Sphaeroma triste is by far the most common species in this area and was found extensively in perforated rocks at all four sites and is abundant at Tusan and Peliau beaches (Table 2). It was also found, but more rarely, in perforated wood that is immobilized in the intertidal zone, such as old bridge supports and large items of driftwood embedded in the beach. The rock perforations, which are the focus of this study, are attributed only to S. triste as no evidence of any other rock boring species was found. Sphaeroma triste is the most abundant and is found exclusively within perforations in rock or wood (except when disturbed), and there is clear evidence that it is the perforation maker in these rocks (see below, description of species). Although S. triste was also found in wood, it does not appear to be the perforation maker in wood. The wood is riddled with dense shipworm perforations. Dynamenella trachydermata was found in wood, on algal covered rock surfaces, and among the sediments in shallow rock pools at Taman Selera beach, but the species is quite rare. It was not found boring into rock or inhabiting the perforations in the rocks, which were found to be exclusively occupied by S. triste at all the sites. The general intertidal habitat for D. trachydermata is thought to overlap somewhat with that of S. triste, but with a tendency to be found lower in the intertidal zone, where red algae, limpets, and small mussels are also more common. The species has previously been recorded in Singapore (Bruce and Wong, 2015). The smaller asellotan isopod species I. singaporensis was found commensal on specimens of S. triste. Iais singaporensis has been previously described commensal on wood-boring specimens of S. triste in West Malaysia (Müller and Brusca, 1992).

Position of Live Isopods in the Rock Perforations

Many, or most, of the perforations in the rock within the intertidal zone are occupied by isopod individuals, all of which are S. triste species. When undisturbed, the live isopods are most commonly positioned with their anterior end facing the blind end of the shaft (Figures 3 and 4), and their exopods, which extend beyond the posterior margin of the pleotelson, are visible close to the orifice of the shaft. When disturbed, the isopods turn around and may exit the shafts or roll up inside. It is not uncommon to observe two individuals in the same shaft (Figure 4). Occasionally borings are occupied by a group of numerous juveniles. In the upper intertidal zone and in the splash zone, there are also numerous abandoned uninhabited isopod borings.

Figure 4

Detail of freshly broken soft sandstone rock at Tusan beach in NW Sarawak, Malaysia, showing numerous burrows occupied by the isopod Sphaeroma triste. The animals are predominantly positioned with their heads toward the blind ends of borings. Some borings are occupied by more than one individual (at arrow for example). Coin is 18-mm diameter. The original rock surface prior to breakage was approximately parallel to the top of the photo.

Morphology of the Rock Borings by S. triste

At the scale of the rock outcrop, there is no preferred orientation, but a strong tendency for the borings to be generally perpendicular to the rock surface occurs at the bore orifice (Figure 4). In any one area of the perforated zone, the majority of the bore shafts are subparallel with infrequent shafts at a slightly different angle (Figure 4). There is no crosscutting or branching of the borings, which are all simple hollow tubes. Two closely spaced adjacent shafts may be connected where the thin wall between them has been breached or eroded. The perforations are essentially regular cylindrical shaped with a circular transversal section and parallel to subparallel walls in longitudinal section (Figure 4;  Supplemental Figure 3 (238_coas-36-04-03_s04.tif)). The perforations end in a hemispherical termination at the blind end. The isopods are able to curve around their transversal axis to exit their boring (Figure 5). No obvious changes occur in the cross-section diameter from orifice to blind end, with no swellings or taperings (Figure 4). The isopods fit relatively tightly inside their borings, with only a small gap between the animal's body and the shaft wall (Figure 5). The spacing between adjacent borings is variable depending on infestation density at the site, but it is commonly less than several millimeters and as little as ∼150 microns, with possibility of breaching of the wall, i.e. two adjacent borings becoming connected. The borings' diameters are generally well sorted in size, with most falling in the 3.0- to 4.0-mm range. Maximum observed diameter was 4.85 mm. When compared with the average width of adult specimens, which is 4.0 mm, the typical shaft diameters appear low. It is likely that some perforations were formed by smaller individuals than those sampled and/or that the isopod body fits very snuggly in its boring. This appears to be the case, as observed under microscope and in field. It is also possible that the isopod bodies are more curved transversally (at coxal plate sutures) when live in their borings than when examined in the laboratory. The length of the borings is variable, most commonly around 2 cm, with maximum length exceeding 3 cm. This is several times the length of the adult S. triste body. At low tide, the isopod body does not generally protrude outside the bore, although the endopod and exopod in particular may be visible close to the orifice of the boring and extending beyond apex of pleotelson ( Supplemental Figure 3 (238_coas-36-04-03_s04.tif)). Borings that are actively occupied by isopods have clean, smooth walls with no obvious deposits, fill material, or other irregularities (Figures 4 and 5;  Supplemental Figure 3 (238_coas-36-04-03_s04.tif)).

Figure 5

Thin section of sandstone with three isopod borings, one of which contains an isopod in longitudinal section and partially rolled (top image is in plain polarized light, and bottom image is in crossed polarized light). Scale bars are 1 mm. The cross-section is not exactly perpendicular to the axis of the boring, hence it appears oval rather than round. Note: The section passes through one of the isopod's mandible incisor processes that shows a blunt shape (visible in top photo). The black blobs within the isopod's body are where 800-grit carborundum polishing powder has penetrated the body cavities. Both images are a mosaic of 12 individual photos taken with the microscope's lowest magnification (50×) to cover a total field of view of approximately 6 mm by 5 mm.

DISCUSSION

Sphaeroma triste has previously been described from many localities in the Central Indo-Pacific biogeographic realm, where it is considered a native species. The localities range from Lakshadweep Archipelago (off the west coast of India) (Nair and Salim, 1994) to Queensland, Australia (Harrison and Holdich, 1984), which is from latitude 11° N to 27° S and from longitude 72° E to 153° E across much of Central Indo-Pacific. Hence, it is not surprising to find it on the coast of North Sarawak, as reported here for the first time.

This study has shown that rock boring by S. triste is common in soft sandstone rocks in the intertidal zone along the coast of North Sarawak, although the distribution is very localized, generally ranging from nil on unsuitable rock surfaces to a density that commonly reaches four to seven perforations/cm² . Hence, the presence of rock-boring isopods, where it occurs, has a significant erosive effect by direct removal of 20% to 50% volume of rock from the intertidal outcrop surface. Within maximum density zones, where up to 11 perforations/cm² may occur, this is equivalent to the removal of up to 51% to 54% from the top 2 to 3 cm of rock. On the regional scale, however, the volume of direct rock removal is much less because of the highly localized distribution of isopod perforations, which are estimated to occur on significantly less than 10% of intertidal exposed rock.

In addition to the direct action of isopods, the presence of the perforations also has an indirect effect on erosion. The perforations increase the surface area of rock exposed to erosion and significantly weaken the outer few centimeters of the rock mass in these soft clastic rocks. It is noted that the remnant walls of rock between adjacent perforations are thin, often reduced to millimeters or less. This is likely to enhance the effect of other agents of erosion operating in this part of the intertidal zone. Evidence of this is shown by originally cylindrical perforations being reduced in length to their hemispherical blind ends (Figure 3, red circle) and their lateral walls being eroded leaving a half tube (Figure 3, blue rectangle). Isopod perforations contribute to formation of wave-cut notch, to localized enlargement of joints and concavities of the rock surface, to widening of rock pools as well as to gradual destruction of fallen boulders and blocks. Evidence of this enhanced erosion is obvious in numerous rock surfaces showing eroded isopod perforations. The clustered isopod perforations also contribute to the formation of wave-cut notch. Similar bioerosive effect with enhanced cliff erosion and notch deepening has been documented by Cadée, Checa, and Rodriguez-Tovar (2001) in Spain. They estimated that in the case of a cliff comprising fine-grained clastic rocks along the Atlantic coast, up to 40% of the upper 5 cm of cliff was open because of bioerosion by Paragnathia isopods and the Bledius beetle. The burrowing effect of S. quoianum in peat and mud has been reported to reduce stability of marsh bank sediments in San Diego and San Francisco Bays, leading to enhanced erosion attributable to undercutting and collapse of the banks (Talley, Crooks, and Levin, 2001). This differs from the Sarawak situation, as no undercutting or collapse effect was found associated with S. triste borings in sandstone rocks of this study. Two criteria appear to control the localized distribution of S. triste perforations within the upper intertidal zone: rock hardness and shelter from desiccation and/or exposure to sunlight. The latter could explain their presence on joint surfaces and rock-surface concavities. However, it is uncertain if this is entirely because of habitat preference or the result of erosion of already perforated rock surfaces, leading to formation and enhancement of the concavities, or a combination of both. The distribution of perforations does not appear to be related to the intensity of wave action.

The rock borings by S. triste are nonbranching, cylindrical perforations with circular cross-section and hemispherical blind end. They are of variable length, often over 2 cm, and their diameter is generally between 3 and 4 mm. The dimensions are smaller than those of burrows created by the invasive species S. quoianum, which forms burrows of 5- to 7-mm width in peat and mud (Davidson and de Rivera, 2012; Talley, Crooks, and Levin, 2001). Rotramel (1975) reports that Sphaeroma species turn on their longitudinal axes while burrowing, which produces a nearly cylindrical burrow, as appears to be the case here. Sphaeroma triste borings are simple with no enlargements or other features. This contrasts with the burrow complexity reported for S. terebrans in mangrove wood (Messana et al., 1994; Thiel, 1999) as well as the branching and interconnectivity of S. quoianum burrows in peat and mud (Talley, Crooks, and Levin, 2001). Messana et al. (1994) also report that the young S. terebrans dig holes on the internal surface of the adult's burrow. No branching, complexity, nor diggings on the internal surfaces were observed in S. triste borings. In terms of neoichnology, the rock borings of S. triste are considered to belong to the Trypanites ichnofacies (Buatois and Gabriela Mángano, 2011); they are sharp walled and formed in lithified substrate (hard ground). They are deep-tier borings in the sense described by Bromley and Asgaard (1993) because they penetrate the rock to over 2-cm depth as opposed to shallow rasping and etching marks on the rock surface. As mentioned previously, isopods are more commonly known for their wood boring and hence would generally be associated with the Teredolites ichnofacies (Gingras, Maceachern, and Pickerill, 2004).

For S. quoianum, individual and burrow densities of up to tens of thousands per square meter are not unusual (Talley, Crooks, and Levin, 2001). The data from Sarawak suggests that for S. triste in areas of high density in the intertidal zone where habitat is suitable, there might typically be four to seven perforations per square centimeter, or 40,000 to 70,000/m². This study indicates that maximum crowding limit for S. triste is 11 individual perforations per square centimeter, and this could lead to direct removal of approximately 50% of the outer 3 cm of rock, which is approximately 15 L/m². At more typical density of perforations, direct removal would be about half of that. Experimental studies indicated that 100,000 adult S. quoianum could remove 72 L of sandstone in two months from a similar surface (Davidson and de Rivera, 2012). This study did not measure the time required for isopods to create the borings and/or the rate of further penetration of the bioerosive front into the rock mass as the external perforated zone is eroded. Davidson, Rumrill, and Shanks (2008, p. 149) indicate that S. quoianum has the ability to “rapidly colonize intertidal substrata and in a matter of weeks completely riddle wood and other substrata.” The purpose of boring activity by S. triste has not been investigated in this study. In general, boring and burrowing by isopods may be for defense from predators, protection from environmental stresses at low tide, for feeding, for mating and reproduction, or a combination of these (Cragg, Pitman, and Henderson, 1999; Davidson, Rumrill, and Shanks, 2008; Talley, Crooks, and Levin, 2001). In the case of North Sarawak populations, the position of the borings suggests that they provide protection from desiccation, from sunlight exposure, and possibly also from wave agitation. Negative photo-taxis and preference for concavities has also been noted in wood boring by S. terebrans (Messana et al., 1994). Rotramel (1975) noted that the body position of S. quoianum within shafts is consistent with a filter-feeding mechanism as the movement of the pleopods creates a current over and then under the animal. Wood-boring species of sphaeromatids are reported to be filter feeders, but it is believed that they use their burrows as a dwelling place for protection rather than as a food source (Aung Si, Bellwood, and Alexander, 2002; Brusca and Iverson, 1985; Cragg, Pitman, and Henderson, 1999; Rotramel, 1975; Talley, Crooks, and Levin, 2001). Sphaeroma terebrans is reported to perform parental care, with juveniles inhabiting small pockets within the parental burrow or branching off into their own burrows (Messana et al., 1994). Those authors report 15% of burrows were occupied by couples and 5% by families. This study in Sarawak did not address population composition or ecology; however, it is common to find several individuals in one boring and some borings contain groups of juveniles. The lack of isopod boring or perforations in mudstones suggests that the presence of clay in the isopod dwelling may be a limiting factor for S. triste and that there is a preference for soft sandstone. It is not known at which stage of life the individuals start to bore, how long it takes an isopod to excavate a perforation, and whether boring is performed year round or if it is seasonal.

Further research would be required to clarify exactly how S. triste performs the boring in rock, but the blunt mandibular incisor process of the Sarawak specimens is a strong indication that the mandibles are used. It is likely that the incisor processes become blunted by abrasion from contact with angular quartz grains of the rock during this boring. To the authors' knowledge, this blunting has not been described previously.

CONCLUSIONS

In Northern Sarawak, the species Sphaeroma triste was found to be a common rock borer, with heavy infestations and significant bioerosion observed at several sites where soft sandstones and siltstones of Miocene age outcrop in the intertidal zone. The S. triste community has been present and well established here since at least 2007 and perhaps much longer. The Sarawak specimens' morphology match that of northern specimens from New Guinea described by Harrison and Holdich (1984) with four tubercles on the pleotelson. The incisor processes of the adult Sarawak specimens were found to generally be blunt and rounded, not bifid, and this is inferred to be a specific consequence of abrasion attributable to rock boring in sandstone reported here for the first time. In addition to abundant S. triste, two other isopod species were also observed: D. trachydermata (infrequent, not rock boring) and I. singaporensis (commensal on S. triste).

The distribution of isopod rock borings in the north Sarawak coast covered by this study shows high abundance but low diversity because only one species, S. triste, was found to be rock boring. Distribution is localized and dependent on rock hardness, which appears to be a limiting factor. There are few or no borings in hard sandstone or where mineralized crusts have formed on the rock surface. The latter may be colonized by barnacles. The position of the isopod borings on the rock surfaces suggests that the borings provide shelter from environmental stresses of desiccation and strong sunlight during low tide. The S. triste borings are commonly located in the upper half of the intertidal zone and more rarely in the splash zone. Average densities of four to seven borings per square centimeter are common in highly infested areas. The maximum crowding limit appears to be 11 perforations per square centimeter of rock surface. The borings are nonbranching, almost straight round cylinders of 3 to 4 mm diameter. They are approximately perpendicular to the rock surface, which may be horizontal, sloping, vertical, or overhanging. The borings have hemispherical blind ends and have variable lengths with some over 3 cm long. During low tide, the isopods inhabit the borings with their heads pointing inward toward the blind end; it is common to find more than one individual in a single boring, and some borings contain groups of juveniles. Although the effect of boring on the erosion rate has not been fully quantified, in areas of highest abundance the organisms are capable of directly removing as much as 20% to 50% of the outer few centimeters of rock. This bioerosion has an indirect impact on other forms of erosion and leads to deepening of concavities on the rock surface, widening of joints and rock pools as well as enhancing the formation of a wave-cut notch and erosion of fallen blocks. As erosion removes weakened perforated surface material, bioerosion may continue because the isopods bore deeper into the substrate.

Further research is warranted to better understand the regional distribution of this and other isopod species as well as to quantify their bioerosive activity, in particular the rate of infestation and the pace of boring as well as to establish any seasonal variations of the activity. Preservation of rock borings by Sphaeromatid isopods in the rock record, similar to that of other deep-tier endolithic organisms, may have the potential to facilitate identification of fossil rocky shores in ancient stratigraphic sequences, and hence this research is of neoichnological interest. However, their indirect enhancement of mechanical erosion may lead to relatively poor preservation in the rock record. Furthermore, the capacity of Sphaeromatids, some of which are invasive species, to damage manmade timber structures justifies further studies into their ecology and habitat preferences.