Understanding enrolment behaviour in Chitons.

The ability of armoured animals to roll into a defensive ball is known from many disparate groups. This ability, called conglobation or enrolment, is known from Mammals such as Pangolins, Manidae, and Hedgehogs, Tenrecinae, and Echidna, Tachyglossidae, Arthropods including some Isopods, Trilobites, Pill Millipedes and larvae of other groups, and, among Molluscs, the multi-shelled Chitons. These animals have the flexibility to curve their entire body and touch the anterior to the posterior end, such that the hard dorsal elements cover the whole outer surface and the softer, ventral parts are protected inside the ball. Species with this ability span a broad variety of ecological niches and both terrestrial and aquatic environments; while the ability to display protective armour in every direction is doubtless beneficial to defence, the ability to become more spherical may have additional and more relevant implications in terms of functional morphology. Chitons are unusual among ball-forming invertebrate animals in that they entirely lack mechanisms that lock the body in the enrolled position. By contrast, many Trilobites, Oniscoid Isopods and Millipedes have intricate locking (or coaptive) devices that are modifications of the exoskeleton. Many of these ball-forming taxa with coaptive devices protect legs, antennae and reproductive structures, and at least some develop spines that protrude outward when the animal is in the enrolled position. Spines provide an additional defence against gape-limited predators, and in aquatic contexts may affect hydrodynamic dispersal. Conglobation with coaptive devices is common among living terrestrial arthropods, but is essentially unknown in living adults in the sea, perhaps implying that passive defence in the form of coaptive rolling up into a ball is no longer as effective as it once was during the Paleozoic heyday of the Trilobites.

In a paper published in the journal Biology Letters on 2 October 2019, Julia Sigwart of the Marine Laboratory at Queen’s University Belfast, Geerat Vermeij of the Department of Earth and Planetary Science at the University of California, Davis, and Peter Hoyer, also of the Marine Laboratory at Queen’s University Belfast, present the results of a study in which they  applied an experimental approach to test the response of dislodged Chitons with and without exposure to the threat of potential predation.

A Chiton attached to the substratum by its soft foot is well defended by its dorsal scleritome and will respond to disturbance by holding fast to the surface. The Chiton scleritome and its overlapping plates have been analysed as an armour that optimizes a trade-off between defence and mobility. When rolled into a ball, the valves and girdle together provide a complete armour, although much of the ‘ball’ is muscular tissue covered only by a thin cuticle. The potential predators in modern shallow marine settings, including Fish, Seastars, Birds and Crabs, are likely to consume an unattached Chiton whole. Anecdotal speculation has suggested the primary advantage of curling into a ball could instead be mobility, to allow Chitons to roll to a better position. This implies that enrolment is not a passive defence against attack, but perhaps a strategy to improve circumstances. If the tendency of armoured marine animals to roll into a ball is a passive defensive behaviour, then Chitons could be expected to spend relatively more time curled up in the presence of a predator, but if it is not then Chitons should spend less time enroled when a predator is nearby.

A Chiton, Mopalia swanni, in (a) in normal position, and (b) rolled into a ball, anterior is at top in both images. This species was not used in this experiment but shown for illustrative purposes. Sigwart et al. (2019).

Live Chitons were collected from the intertidal at Pinnacle Gulch in Bodega Bay, California and held in aquaria on flowthrough seawater at the University of California, Davis' Bodega Marine Laboratory. Chitons used in these experiments included three species: Mopalia hindsii (17 seventeen specimens), Mopalia muscosa (4 specimens), and Lepidozona mertensii (3 specimens). These species co-occur in the rocky intertidal in Northern California and are broadly distributed on the Pacific coast of North America. The Purple Sea Star, Pisaster ochraceus was selected to produce the predator cue as it is a co-occurring predator known to consume Chitons.

In each trial, a single randomly selected Chiton was placed up-side-down in the centre of the experimental aquarium. Seawater was siphoned continuously from one of two sources, selected by a coin flip: the 40 litre holding aquarium with captive Chitons (control condition), or a separate 20 litre aquarium holding a single Purple Sea Star (predator treatment). These two source aquaria were fed continuously with flow-through seawater. 

Chitons left up-side-down on a flat surface were never able to right themselves, except by manoeuvring close enough to the wall to contact and attach to the vertical surface. This occurred four
times in 24 trials, three of which were in the presence of the predator cue; the control animal that made contact with the side did so only after 109 minutes of a 120-minute trial, while animals in the predator treatment that manoeuvred themselves to the side did so relatively much faster, after 43–87 minutes.

Left in a prone orientation, Chitons adopted the enrolment position around 30% of the time overall; however, there was a strong association between the predator cue and time spent arching. The odds of an individual spending time in a ball are 2.85 times higher without a predator cue. In the presence of a predator cue, the odds of an individual Chiton spending time arching are 2.93 times higher. 

The sample sizes for Lepidozona mertensii (3 specimens) and Mopalia muscosa (4 specimens) were too small to allow robust comparison among species, although the trends were apparently broadly consistent in all three species used. Lepidozona mertensii spent more time overall curled into a ball, compared to the total group, and spent considerably more time rolled in the control condition  than in the presence of a predator cue.

In the presence of the chemical cue of a distant predator, the urgent pressure to reattach to the substratum prompted more exposed positions in Chitons, but that would (and in a few cases did) enable the animal to reattach to the substratum and regain normal posture. Chitons are not able to right themselves on an isolated, flat surface such as the bottom of an experimental aquarium. But extended flat surfaces and still water are unusual in the context of rocky marine benthos. The articulating armour of Chitons is flexible and the inability of chitons to right themselves is generally limited to environments with flat surfaces and no current. In normal circumstances, on a rugose surface in a dynamic environment with moving water, a rolled-up chiton can expect to be transported to a new position very rapidly, and an arching Chiton might also be buffeted more rapidly toward a potential safe haven. Although Chitons are often considered ‘primitive’, there is mounting evidence for neurological complexity and this behaviour suggests a certain level of strategic response.

The behaviour associated with conglobation has been studied most closely in Arthropods, especially the terrestrial Pill Bug, Armadillidium sp., which can roll into a completely sealed ball. In experimental exposure, Isopods were marginally more likely to be attacked when extended rather than when rolled into a ball, and the animals do use conglobation as an active response to attack by potential predators. Likewise, a dislodged Chiton, if physically prodded, would also roll up rather than arch and leave the foot exposed. Conglobation in Isopods has secondary advantages in that it may help prevent desiccation as well as predation, which would only be relevant for Chitons in the rare event of dislodgement when exposed to air at a low tide. There are certainly protective benefits to curling into a ball, but the ball configuration in Chitons and other animals is entirely incompatible with normal feeding and locomotion.

Some arthropods lack coaptive devices that lock the ball configuration, including a few terrestrial Caterpillars and Spiders. These animals roll into a wheel-like configuration and use powerful appendages to propel themselves away from danger. This situation, and the observation that the ability to roll into a ball is associated with rolling away from a disadvantageous situation rather than with direct or even indirect contact with a predator, is mirrored in Sigwart et al.'s observations of chitons. Whether energy-intensive as in these terrestrial Arthropods, or more passive, as in Chitons, rolling away evidently does not require coaptive devices and is more a temporary measure.

In Chitons, the action of enrolment is controlled by the diagonal dorsoventral muscles that connect the eight shell valves to the ventral foot. All Chitons are able to use anterior–posterior flexing, including species with reduced or internal shells (such as Cryptochiton stelleri). This muscular arrangement and additional longitudinal muscles also cause the typical curled posture in Aplacophoran Molluscs, which are anatomically and phylogenetically related to Chitons. This is in contrast to the coaptive interlocking exoskeletal elements involved in the conglobation postures of Arthropods. Although the shell-less condition in Aplacophorans is derived, curling does not require an exoskeleton and does not require physical coaptive devices.

The ability of animals to transform into a defended sphere is a solid defence with multiple benefits; however, the results here suggest that anti-predatory defence is not the principal merit for Chitons. Chitons demonstrate behavioural decision-making when faced with the threat of a potential predator, to enable it to right itself and regain a safe foothold. By contrast, some other species with coaptive mechanisms resist attack by a predator through special morphological features that strengthen the exoskeleton and make it difficult to manipulate for a gape-limited or skeleton-breaking predator. The rolled-up configuration in Chitons and other animals without coaptive devices is superficially convergent, but the similarity in these different forms of rolling up may hide fundamentally different approaches to defence.

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Shellfish use at the Oakhurst Period at Klipdrift Cave, South Africa.

Early evidence for the exploitation of Shellfish for subsistence traces back to at least 164 thousand years during the Middle Stone Age in South Africa, and by 100 000-60 000 years ago Shellfish were systematically and intensively exploited at a handful of sites. Evidence for the use of Shellfish for purposes other than food, such as making containers and ornaments, appears from 100 000 to 75 000 years ago in the southern Cape. It is, however, possible that many older sites containing Shellfish remains were destroyed by the Marine Isotope Stage 5e sealevel transgression (between 124 000 and 119 000 years ago,  the last interglacial period before the present, when global mean surface temperatures were at least 2°C warmer than today and mean sealevel was 4–6 m higher than at present, following reductions of the Greenland ice sheet). Furthermore, there is little evidence for shellfish exploitation between 50 000 and 14  000 years ago, mainly because of the paucity of coastal sites from this time period (during the last glacial maximum, when sealevels were as much as 125 m lower than today, with the effect that most coastal areas in Southern Africa at the time are now bellow sealevel). Evidence for Shellfish use re-appears at around 14 000 years ago in the southern Cape, at the end of the period associated with the Robberg techno-complex. Shellfish become more abundant in sites during the subsequent period linked to the Oakhurst techno-complex, around 14 000 to 7000 years ago, although sites from this period with shellfish are still relatively uncommon. The most abundant evidence for intensive Shellfish exploitation in South Africa comes from the ‘megamidden’ period, between 3000 and 2000, from the West coast, which is dotted with extensive open shell middens.

In a paper published in the South African Journal of Science on 26 September 2019, Kokeli Ryano of the Department of History at the University of Dodoma, Karen van Niekerk of the Centre for Early Sapiens Behaviour at the University of Bergen, Sarah Wurz, also of the Centre for Early Sapiens Behaviour at the University of Bergen, and of the School of Geography, Archaeology and Environmental Studies at the University of the Witwatersrand, and Christopher Henshilwood, again of the Centre for Early Sapiens Behaviour at the University of Bergen, and the Evolutionary Studies Institute at the University of the Witwatersrand, present new data on Shellfish exploitation during the Oakhurst Period from a recently excavated Later Stone Age site, the Klipdrift Cave, in the southern Cape.

The term Oakhurst techno-complex is used here for sites that typically date to between about 14 000 and 7000 years ago, and that follow the Robberg techno-complex, although regional variants occur across southern Africa. Furthermore, the transition between entities such as the Robberg and Oakhurst in the Cape region was not synchronous. The Oakhurst is characterised by non-microlithic and bladelet poor lithic assemblages dominated by unstandardised flakes, and frequent use of coarser grained lithic raw materials. Formal tools are rare and consist mainly of medium to large scrapers. Non-lithic artifacts associated with the Oakhurst include worked bone, Ostrich eggshell beads and ornaments as well as worked marine shell and beads. The Robberg period is characterised by relatively few Shellfish remains, but during the Oakhurst, Shellfish, Fish, Marine Mammals and Seabirds are present in the deposits. Initially the Oakhurst people also hunted large-to-medium-sized game such as Eland and Warthog, but these prey were later replaced by browsers, likely reflecting a change towards a woodier habitat. 

Of the eight securely dated Oakhurst sites in the southern Cape, four, Nelson Bay Cave, Matjes River Shelter, Byneskranskop 1, and Oakhurst Shelter, contain significant Shellfish remains, probably because they were close to the coast. At inland sites such as Boomplaas Cave, and Kangkara Cave, Wilton Large Rock Shelter, and Melkhoutboom Cave, Shellfish are rare, and, when present, may have predominantly been used for non-subsistence purposes such as the manufacture of ornamental and decorative items.

Sites containing material from the Oakhurst Complex in the southwestern Cape. Kokeli et al. (2019).

The shellfish from three of the four sites have been described to varying degrees. The Shellfish from Oakhurst Shelter were listed to species level but not quantified, and Shellfish samples do not appear to have been retained during the initial excavations, which took place in the 1930s. It is, however, evident that the White Sand Mussel, Donax serra, is the most common species in the Oakhurst levels.

Nelson Bay Cave and the Matjes River Shelter are situated approximately 10 km apart with similar rocky shores and sandy beaches in close vicinity. The most common Shellfish species in the Oakhurst levels are the Brown Mussel, Perna perna, White Mussel, Donax serra, and Black Mussel, Choromytilus meridionalis. At both sites, there is an inverse correlation in the frequency of these species over time (i.e. Shellfish use becomes less frequent as time passes). At Nelson Bay Cave Choromytilus meridionalis is replaced by Perna perna around 10 000 years ago whilst Donax serra frequencies increase at the same time. At the Matjes River Shelter Perna perna increases sharply relative to Choromytilus meridionalis by 9500 years ago, but, unlike at Nelson Bay Cave, Donax serra is most common in the earlier layers, dated to about 10 000 tears ago, and decreases as Perna perna increases. These changes in species representation over time have been interpreted as indicative of changing environmental conditions.

At Byneskranskop 1, Shellfish are present in the Oakhurst layers in relatively low frequencies; the total minimum number of individuals. is 310. The frequencies gradually increase from the oldest 13 000 year old to the youngest 7000 year old Oakhurst layers, but only become significantly abundant in the overlying layers attributed to the Wilton Period. The low numbers probably reflect an increased distance from the shore prior to the Wilton. Numbers of Choromytilus meridionalis and Perna perna are negligible, although the former outnumbers the latter in all the Oakhurst layers. Donax serra is the most common species in all but the youngest Oakhurst layer, dated to 7000 years ago, where the Alikreukel, or South African Turban Shell, Turbo sarmaticus, become more common. It is unclear whether Donax serra shells were brought in primarily as food, as some perforated fragments were found, which may suggest that they had been used as artefacts. Modified Donax serra shells have not been reported from Nelson Bay Cave or the Matjes River Shelter.

It has been argued that the sizes of Gastropods, and variation in Shellfish species, from archaeological sites may provide an estimate of the extent and intensity of harvesting of these animals as food, which in turn can be used as a reflection of Human population size. The reduced size of Gastropods in Late Stone Age sites relative to those from Middle Stone Age localities in Southern Africa has been used to imply intensified collection due to higher human population size during the Late Stone Age. In addition, Middle Stone Age assemblages tend to contain a smaller range of mostly larger species, and the few smaller species tend to occur in low numbers relative to Late Stone Age assemblages. As such, Gastropod size and species abundance have been used to argue for smaller Human population sizes during the Middle Stone Age. Another argument is that the reduced Gastropod size could be due to environmental factors affecting shell growth rates, particularly as non-food species are also reduced in size in the Late Stone Age compared to Middle Stone Age. It is also interesting that data on the Tessellated Nerite Snail, Nerita tessellata, from the Caribbean island of Nevis indicate that shellfish size increased despite intensive exploitation by Human populations between 890 and 1440 AD.

The Klipdrift Cave is located on the coast in the De Hoop Nature Reserve in Swellendam District in the southern Cape, South Africa. It forms part of the Klipdrift Complex where Klipdrift Shelter, a Howiesons Poort locality, dating from about 70 000 to about 50 000 years ago, is also found. The Klipdrift Cave was first excavated in 2010 and subsequently in 2011. The surface of the deposit in Klipdrift Cave is truncated, possibly by mid-Holocene higher sea levels, but excavations over an area of 2.75 m² revealed horizontal in-situ depositional layers with exceptional preservation of bone, shell, charcoal and Ostrich eggshell. The lithics are assigned to the Oakhurst techno-complex, and the top and bottom of the excavated sequence have been dated to approximately 10 000 and 13 000 years ago, respectively.

The Klipdrift Complex (Klipdrift Cave is the western section and Klipdrift Shelter is to the east). Kokeli et al. (2019).

All the shellfish remains retained in the 3-mm sieve from layers JY (between about 10 760 and about 11 170 years old) through KAE (between about 13 480 and about 13 740 years old), which form 85% of the total excavated volume (0.93 m³) at Klipdrift Cave were analysed. Whole Shellfish smaller than 2 cm were not considered to be food items but rather animals that landed up in the site incidentally, for example through attachment to bigger shells, and were not included in this analysis.

The methods and techniques adopted for analysing marine Shellfish from Klipdrift Cave involved species identification, determining the minimum number of individuals, weighing the shells, and measurements of the maximum ‘length’ of Turbo sarmaticus opercula and Limpet shells. Both minimum number of individuals and weight are used as rare species may be underrepresented when only minimum number of individuals is used, and further because post-depositional damage can affect the minimum number of individuals counts.

Minimum number of individuals counts for Turbo sarmaticus are derived from counting apices and opercula and the highest value is considered the minimum number of individuals. The weight for Turbo sarmaticus used includes the opercula and shell weights. The minimum number of individuals values for other Gastropods are calculated by counting the apices. For the Giant Chiton, Dinoplax gigas, the front, middle (the number of middle valves divided by six), and rear valves were counted separately, and greatest total for the three categories was taken as the minimum number of individuals. Left and right hinges of Bivalves were counted separately, and the highest value taken as the minimum number of individuals.

Eleven Mollusc species with a total minimum number of individuals of 5330 were identified from 197.69 kg of Shellfish remains. Two Periwinkle species, Diloma sinensis and Diloma tigirina, are present, but, as the apices are usually separate from the identifiable body whorl, the shell weights and minimum number of individuals have been combined for these two species and listed as Diloma spp. No shell fragments of Diloma variegata were found, and it is therefore assumed that only the former two species are represented by the apices of this family at Klipdrift Cave. All the species identified still occur in the southern Cape today, and no cold-water indicator species (such as the Granite Limpet, Cymbula granatina) are present.

All species found are edible, and most were presumably collected primarily as food. It is possible that the White Mussels, Donax serra, were first eaten, and some shells subsequently used for other purposes, as 14 of the valves have roughly 10 mm circular perforations near the centre. The Angular Surf Clam, Scissodesma spengleri, present in small numbers throughout the sequence, may also have been used for purposes other than food. This species occurs subtidally in the deeper surf zone, and is therefore difficult to collect live but specimens do wash up after storms. The Klipdrift Cave specimens do not appear waterworn, but these washed up shells are seldom damaged or waterworn. Thus, it is not clear whether these specimens were collected dead or alive. Some of the valves have what appears to be retouch on the ventral side, and might have functioned as a sort of scraper, but this possibility needs further investigation. Incidental, nonfood species consist mostly of Barnacle fragments and juvenile Limpets.

The South African Turbam Shell, Turbo sarmaticus and the Giant Chiton, Dinoplax gigas, are the most frequently occurring species throughout the assemblage, contributing over 93% in terms of minimum number of individuals and 95% in terms of weight. All other species combined contribute less than 4% in terms of weight, and 7% in terms of minimum number of individuals to the total assemblage. Brown Mussel, Perna perna, Abalone, Haliotis midae, Venus Ear, Haliotis spadicea, Long-spined Limpet, Scutellastra longicosta, and Surf Clam, Scissodesma spengleri, occur in negligible numbers. Goat’s Eye Limpet, Cymbula oculus, Periwinckle, Diloma spp. and Whelk, Burnupena cincta, occur in slightly higher numbers than the aforementioned, but still at very low frequencies relative to Dinoplax gigas and Turbo sarmaticus.

Dinoplax gigas is the most abundant species in the site, both in terms of weight and minimum number of individuals. There is an inverse relationship in frequency between Dinoplax gigas and Turbo sarmaticus through time, with the former being most abundant in the lower part of the sequence (layers KAE–JZB; i.e. layers between about 13 740-12 735 years old), and the latter in the upper four layers (JZA–JY; roughly 13 000-11 170 years old). On a much smaller scale, the frequencies of Burnupena cincta, Cymbula oculus, and Diloma spp. follow a similar pattern: Burnupena cincta is most common in the lower layers associated with Dinoplax gigas and all but disappears in the upper layers, whereas the relative frequencies of Cymbula oculus and Diloma spp. increase in the upper layers. Donax serra is present in all layers in low numbers, but its relative frequency is highest in the same layers where Burnupena cincta is most common. 

Part of the Klipdrift Cave natural stratigraphic profile and associated accelerator mass spectrometry dates. Kokeli et al. (2019).

Brown Mussels, Perna perna, are absent from the lowermost two layers and layer JZA, and constitute only between 0.2% and 2.2% of minimum number of individuals in the layers in which they do occur. Abalone, Haliotis midae, Venus Ear, Haliotis spadicea, occur in negligible quantities, but it is notable that they are only present in layers above JZB  (i.e. younger than 13 000 years old), except for a few fragments in KAB (less than 13 400 years old).

Klipdrift Cave contains a limited number of species (11) relative to the other sites, particularly Matjes River Shelter (20). Some Shellfish species, such as the Ribbed Mussel, Aulacomya atra, Kelp Limpet, Cymbula compressa, and Granite Limpet, Cymbula granatina, are restricted to one site (Matjes River Shelter). Limpets are rare at Klipdrift Cave and Byneskranskop 1 and more common at Nelson Bay Cave and Matjes River Shelter. Surf Clams, Scissodesma spengleri, are present only at Klipdrift Cave and Byneskranskop 1.

Shellfish densities at Klipdrift Cave are very high in the three uppermost and two lowermost layers of the sequence. Densities are the lowest between layers KAC (between 13 375 and 13 560 years old) and JZA. Layer KAD (less than 13 400 years old) has the highest shell density, at~374 kg/m³, and JZB (less than 12 735 years old) the lowest, at ~28 kg/m³. Caution should be taken when using density measures, particularly when making inter-site subsistence comparisons. However, as Klipdrift Cave is a ‘closed’ cave (as opposed to open air sites), intra-site density comparisons are less likely to be significantly problematic, although deposition rates may have differed between layers.

The southern Cape species most frequently used for size measurements are the various Limpets and the opercula of Turbo sarmaticus. The latter are used as a proxy for shell size as shells tend to be fragmented in archaeological assemblages. At Klipdrift Cave Opercula lengths range between 10 mm and 48 mm through the sequence. The median value is highest in layer KAD, at 39 mm, and lowest in KAB, at 30 mm. 

Klipdrift Cave measurements were compared with those from other Late Stone Age localities (Blombosfontein, Blombos Cave, and Nelson Bay Cave) and Middle Stone Age sites (Klasies River, Klipdrift Shelter, and Blombos Cave) from the southern Cape. The Blombosfontein level 2 specimens are slightly larger than those from both Klipdrift Cave and Nelson Bay Cave sites while there is a progressive decrease in size of Turbo opercula for younger Late Stone Age sites. The difference in size of specimens between Oakhurst and post-Oakhurst assemblages such as Bloombosfontein level 3 is significant. The general trend is that specimens from Middle Stone Age sites are larger than those from Late Stone Age ones; for example, there is a significant difference between Blombos Cave and Klipdrift Cave.

The most common limpet species present at Klipdrift Cave is Cymbula oculus. As whole (measurable) Cymbula oculus shells were rare (17 specimens), the measurements were combined for all layers. While the sample size was small, Kokeli et al. include the data as a contribution to the available information on Shellfish size patterns during the Oakhurst period in the southern Cape. As with the Turbo sarmaticus measurements, Cymbula oculus measurements from Klipdrift Cave were compared to those from other Middle Stone Age and Late Stone Age sites in the southern Cape. Cymbula oculus specimens from Klipdrift Cave are smaller in size than those from the Nelson Bay Cave Oakhurst layers, with an average size of 62 mm at Klipdrift Cave, and 66.5 mm at Nelson Bay Cave. Cymbula oculus specimens from Middle Stone Age sites such as Klasies River and Blombos Cave are larger than those from Klipdrift Cave by at least 7 mm.

The Klipdrift Cave data present two clear patterns of exploitation: (1) the dominance of Dinoplax gigas in the lower layers, with dates centring on 14 000 and 13 000 years ago and (2) the high frequency of Turbo sarmaticus in the upper layers, from layer JZA up (i.e younger than 13 000 years old). Kokeli et al. question whether this shift in the presence of species is related to changes in sea surface temperatures, habitat change or deliberate human choice.

Shellfish species composition has often been used as an indicator of sea surface temperatures. However, only a few species are effective temperature indicators. These species include Cymbula granatina and Aulacomya atra that occur on the west coast and are indicative of cool temperatures.

Non-food species such as Cellana radiata capensis and Alaba pinnae, indicate warmer waters, but these species do not occur at Klipdrift Cave. The species conventionally used as temperature indicators, Choromytilus meridionalis for ‘mostly cool’ temperatures and Perna perna and Cymbula oculus for ‘mostly warm’ sea surface temperatures, cannot be regarded as reliable proxies for sea surface temperatures. An experimental study has suggested that Choromytilus meridionalis do not thrive in temperatures above 18°C, but Choromytilus meridionalis can co-exist with Perna perna in the south coast surviving in sea surface temperatures above 20°C. This supports the suggestion that Choromytilus meridionalis and Perna perna may not be reliable temperature indicators. Furthermore, there are minor differences in habitat preferences between Choromytilus meridionalis and Perna perna that may cause them to co-exist spatially separated in the same locality. Choromytilus meridionalis, for example, occurs on rocks on the low shore that are associated with sand while Perna perna occurs on the high shore on rocks which are not usually covered by sand.

As most of the species that occur at Klipdrift Cave thrive in both warm and cool sea temperatures, it is difficult to infer sea surface temperatures at the times of occupation. However, the absence of Cymbula granatina, a more reliable cold-water indicator species at Klipdrift Cave, Nelson Bay Cave and Matjes River Shelter suggests that sea surface temperatures in the southern Cape coast were mildly warm during the Oakhurst period.

Species representation can also reflect past habitats. In this regard it is surprising that Choromytilus meridionalis is not present, even in the lower Klipdrift Cave sequence, as the dominant presence of Dinoplax gigas suggests sand inundated rocky shores, a habitat that is attractive to Choromytilus meridionalis. This species is also present at the other Oakhurst sites mentioned. The low incidence of sessile Mussels such as Perna perna at Klipdrift Cave is also unusual as they are typically common in Late Stone Age sites of the southern Cape coast such as Nelson Bay Cave, Matjes River Shelter, and the Blombosfontein sites (which date from between 6000 and 500 years ago).

The fluctuating presence of Dinoplax gigas and Turbo sarmaticus at Klipdrift Cave may be due to changes in the habitat best suited to each species over time. The shift from the dominance of the more sand-tolerant species, Dinoplax gigas, in the lower layers (before 12 000 years ago) to the dominance of Turbo sarmaticus in the upper layers may suggest scouring out of sand in the later period. Turbo sarmaticu would have thrived in a habitat with more exposed rocks and less sand. The near absence of sessile Mussels at Klipdrift Cave may suggest a sheltered sandy bay in front of the cave at times, an environment not favoured by these species. The slight increase in sessile Mussels towards the top of the sequence could indicate a change to rockier shores and rock pools that would also have attracted Turbo sarmaticus and Limpets such as Cymbula oculus.

The subtle changes in coastal morphology suggested by the shifting dominance of the species may have been a result of rising sea levels and is less likely due to changing sea surface temperatures. The rising sea levels signalled the transition from the Last Glaciation towards the Holocene epoch. The complete absence of Haliotis midae and the low incidence of Perna perna and Cymbula oculus (species that do not tolerate overly sandy environments) in the circa 10 000 year old layers support a scenario of a sandy dominated marine environment around this time.

A final scenario to consider for the change of species composition at Klipdrift Cave is whether this change relates to Human choice, acknowledging that it is complicated to discriminate between changes resulting from Human choice and those from the environment. Although the dominant species at Klipdrift Cave prefer slightly different habitats, it is common for them to, at times, occur in close vicinity, suggesting that both could have been available for collection during gathering events.

One possible indication that Human choice was responsible for the difference in representation through time is the size of Turbo sarmaticus in the lower layers. If the coastal zones were newly colonised by this species in the lower layers, then one would expect the population to consist of smaller animals, migrating from crowded subtidal populations, not the larger ones that tend to stay in the lower subtidal areas. While Turbo opercula measurements in the lower layers at Klipdrift Cave indicate a relatively small average size, there are some large individuals present, particularly in layers KAE and KAD. The presence of such large individuals suggests that a mature Turbo population was present and available and could be tentative evidence that people actively chose to collect Dinoplax gigas in the older levels, despite the availability of good sized Turbo sarmaticus. However, it seems more convincing at present to suggest that the shifting dominance of Dinoplax gigas and Turbo sarmaticus at Klipdrift Cave was caused by habitat change rather than Human preference. A similar scenario is suggested for the Middle Stone Age site of Klipdrift Shelter at the same locality, where Dinoplax gigas replaces Turbo sarmaticus and Haliotis midae in the upper layers. This argument may be tested by future research when refined palaeoenvironmental reconstructions of Klipdrift Cave become available. In the instance of Choromytilus meridionalis and Perna perna, it is unlikely that people would discriminate between the former and the latter when collecting, as they are presumably the same in terms of size and taste. Thus, the absence of Choromytilus meridionalis and the rarity of Perna perna may be most likely explained by environmental factors rather than human decision to not collect them.

Shellfish sizes in archaeological sites have been linked to Human population sizes and the intensity of harvesting. Comparison of Shellfish size between Middle Stone Age and Later Stone Age sites in the southern Cape is discussed only for Turbo sarmaticus opercula and Cymbula oculus shell measurements. Given the relative rarity of Cymbula oculus at Klipdrift Cave, their overall small size is unlikely caused by Human predation pressure. There is no criterion established for comparing Dinoplax gigas sizes although they are numerous at Klipdrift Cave, Klipdrift Shelter, and the Middle Stone Age levels at Blombos Cave, and are also present at Matjes River Shelter, between 9600 and 7000 years ago. Comparing their size through time may be a subject for later research.

Turbo sarmaticus opercula from Klipdrift Cave are smaller in size than those from the Middle Stone Age of the Klipdrift Shelter, Blombos Cave, and Klasies River sites, but larger than most post-Oakhurst assemblages from Blombos Cave, Klasies River, and Blombosfontein. The few measurable Cymbula oculus shells at Klipdrift Cave are also smaller than those from Middle Stone Age sites and more like those from the Oakhurst layers at Nelson Bay Cave.

It may be significant that non-food Shellfish such as Tick Shell, Nassarius kraussianus, from the Middle Stone Age at Blombos Cave are significantly larger than those from the Late Stone Age levels at the same site and at Die Kelders. It is unlikely that the reduced sizes of Nassarius kraussianus in Late Stone Age contexts can be attributed to intensive collection as they were not that intensively collected. Hence, the differences in sizes of Shellfish, especially Limpets and the Turban Shells in the Middle Stone Age and Late Stone Age sites, may have been caused by a combination of both natural and Human factors.

Non-Human factors that affect the Shellfish growth rates include sea surface temperature and turbidity, salinity, topography, wave action, desiccation, Shellfish population densities and food supply. Oceanic productivity or the production of organic matter by Phytoplankton, generates food for marine life such as Shellfish. Productivity changed over time and it is known that the primary productivity of the Subantarctic Ocean changed over the last 70 000 years with marked Algal production spikes at about 58 800, 53 000, 46 000 and 38 500 years ago. Oceanic productivity data for the southern Cape coast are not available, but productivity may have been influenced by the Subantarctic Ocean. Variations in oceanic primary productivity affect the food chain and, in turn, may affect size and distributions of Shellfish species. The growth of Turbo sarmaticus is affected not only by lack of food but also by its quality. Changes in oceanic productivity may have resulted in changes in the availability and the quality of food on the southern Cape coast, although this supposition remains to be firmly established.

In the case of the Klipdrift Cave data, to test whether increased predation led to a decrease in size, we predicted size reduction in Turbo sarmaticus from the older to the younger layers, when exploitation of this species intensified. This prediction is based on the premise that a present but unexploited Turbo community will contain many large specimens. It has also been hypothesised that Humans tend to target the largest specimens first when gathering Shellfish and the smaller ones may be collected later and thus the overall size distribution would become skewed. If Shellfish collectors were intentionally seeking out a species at Klipdrift Cave, one would expect the initial assemblage to contain the largest specimens, and a gradual reduction in size through time as increased predation leads to fewer large specimens being available. 

Opercula measurements show that sizes decrease from layer JZA (younger than 13 000 years old) upwards, and the difference in size between JZA and the uppermost two layers, JYA and JY, is statistically significant. Thus, the decrease in size through time of Turbo sarmaticus opercula at Klipdrift Cave, especially after JZA, may support a scenario of intensive exploitation leading to reduction in size. This decrease coincides with an increase in Shellfish densities, which could be because of more intensive harvesting or occupation intensity at this time. However, this does not explain why the Klipdrift Cave opercula are smaller than those in Middle Stone Age contexts. It is possible that Turbo sarmaticus at Klipdrift Cave had slower growth rates than during the Middle Stone Age due to not yet established environmental factors. Although Turbo sarmaticus were rare in the lower part of the sequence at Klipdrift Cave, when presumably little exploitation occurred, they are still smaller than Middle Stone Age ones, which suggests that environmental conditions affected their growth rates.

Although there were probably larger human populations during the Late Stone Age, non-Human factors could also have impacted Shellfish size. Reduced size of Shellfish may also be a function of more frequent harvesting by smaller groups. Until all the causal factors are carefully weaved together, larger Human population as the only driver of Shellfish size reduction is untimely.

Shellfish remains are rare during the Robberg, a period that precedes the Oakhurst, at sites such as Nelson Bay Cave, as sea levels were lower during the Last Glacial Maximum. Shellfish become abundant again from the Oakhurst period and thereafter. The increase in Shellfish subsistence during the Oakhurst period coincides with the rise of sea levels. The sea level transgression after 14 500 brought the coastline very close to the present-day Oakhurst sites on the southern Cape coast. The shellfish species exploited at Klipdrift Cave differ somewhat from those at Matjes River Shelter and Nelson Bay Cave, and changes through time are evident at all three sites. At Klipdrift Cave, for example, there is a change from the dominance of  Dinoplax gigas to Turbo sarmaticus in the sequence after/around 12 000 thousand years ago (from layer JZA), the period that coincides with the driest environment in the sequence as suggested by Ostrich eggshell isotopes. At Matjes River Shelter and Nelson Bay Cave, Perna perna replaces Choromytilus meridionalis about 10 000 years ago. These changes are likely a result of changes in local habitat conditions through time and site-specific shores. The isotopic data from Ostrich eggshells also indicate maximum aridity in the sequence in layer JZA (between 13 000 and 12 735 years old). Furthermore, shellfish density is lowest in layer JZB, which also shows a decrease in lithic production. When these trends are compared to the temperature data for the terrestrial sequence of pollen at Wonderkrate. it is clear that layer JZB (more than 13 000 years old), where the lowest density of shellfish is recorded, coincides with the time when temperatures were probably the lowest during the Younger Dryas. The Younger Dryas event might indeed have had a cooling effect over environments in southern Africa, but the influence of this effect may have varied regionally. On the other hand, the lowest densities of both Shellfish and lithic artifacts at layer JZB may also suggest a low-occupation period at the cave, but this argument needs to be supported by other faunal data.

The change in Shellfish composition probably reflects habitat change that involved removal of sand from the rocks after or around 11 000 thousand years ago due to increasing sea levels. The decrease of the Sand Mussels at Matjes River Shelter and Nelson Bay Cave in the upper layers also supports the shrinking of sandy shores at this time. It is noteworthy that the Shellfish subsistence practises track the change in environment much more closely than the lithic technology does at Klipdrift Cave.

As there are only a few sites in the southern Cape with exceptionally preserved Shellfish remains, Kokeli et al.'s study broadens our understanding and provides new data on Shellfishing during the Oakhurst period. There are inter- and intra-site variations in the shellfish species exploited, perhaps because of subtle habitat changes.

Of the 11 mollusc species that occur at Klipdrift Cave, 2 are dominant: Dinoplax gigas is abundant in the lower layers while Turbo sarmaticus is more numerous upwards. The density of shellfish at KDC is lower in the middle of the sequence, which may be due to sea level regression and/or less intensive occupation of the site at that time. The shift from the dominance of Dinoplax gigas to Turbo sarmaticus may have been caused by rising sea levels, resulting in environmental changes from sand-covered rocky shores prior to 11 000 years ago and more exposed rocks thereafter. The absence of Choromytilus meridionalis at Klipdrift Cave, which is present at both Nelson Bay Cave and Matjes River Shelter during the Oakhurst, and the rarity of Perna perna, may be due to unsuitable habitats for these species at Klipdrift Cave, and not related to sea surface temperatures. Effective sea surface temperature indicator Shellfish species are not present at Klipdrift Cave but the absence of cold temperature species suggests that sea surface temperatures were relatively warm. The terrestrial climate during the Oakhurst at Klipdrift Cave was most likely warm and arid.

The sizes of Turbo sarmaticus opercula and Cymbula oculus from the Oakhurst levels at Klipdrift Cave and Nelson Bay Cave are smaller than those from Middle Stone Age sites. The opercula are larger than in the post-Oakhurst Late Stone Age sites. A combination of factors may explain this scenario better than a single cause.

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