Drilling under threat: An experimental assessment of the drilling behavior of Nucella lamellosa in the presence of a predator

Using the drilling muricid, Nucella lamellosa (Gmelin 1791) and its prey, the mussel Mytilus trossulus (Gould 1850), the impact of a secondary predator, the crab Cancer gracilis, on drilling was investigated experimentally. The frequency of incomplete holes was compared under two conditions: (1) when the gastropod's natural predator, C. gracilis, was present and (2) when it was absent. The results indicate that the presence of a secondary predator can affect drilling activity, leading to a significant increase in the frequency of incomplete drill holes. The introduction of a secondary predator can also decrease the overall drilling frequency. The size distributions of completely and incompletely drilled mussels suggest that in the presence of the secondary predator the decision by the gastropod to either abandon or continue drilling its prey might be influenced by how much time it has already invested into drilling or the size of the prey item. These results are important for the ecological and evolutionary implications of incomplete drill holes frequencies, especially with regard for their use as proxies for evolutionary prey improvement.     

Drill holes in Australian Cainozoic brachiopods

The fossil record of drill holes in marine invertebrates has received a considerable amount of interest from paleontologists, primarily due to its importance for reconstructing the history of interactions between drilling predators and their prey. Such drill holes have been described in numerous studies of Paleozoic brachiopods but rarely in those focusing on brachiopods of the post-Paleozoic, a striking pattern given that in the late Mesozoic and Cainozoic drilling gastropods diversified and frequencies of drilled molluscs increased dramatically. During the past several years, however, drilled brachiopods were reported in several studies of the Mesozoic and Cainozoic, suggesting that this phenomenon may be more common than has been previously assumed. Here we report on 10 genera of brachiopods from four Cainozoic basins in Australia of which 7 shows evidence of having been drilled by predators. Of 298 specimens examined, 38 contain a single complete hole. Drilled specimens were identified in all 4 basins and in all stratigraphic units. When considered in the context of recent reports of drilled Cainozoic brachiopods, these Australian brachiopods further imply that drilling predation on these invertebrates was geographically, taxonomically and temporally widespread.     

Intense drilling in the Carboniferous brachiopod Cardiarina cordata Cooper, 1956

The brachiopod Cardiarina cordata, collected from a Late Pennsylvanian (Virgilian) limestone unit in Grapevine Canyon (Sacramento Mts., New Mexico), reveals frequent drillings: 32.7% (n = 400) of these small, invariably articulated specimens (<2 mm size) display small (<0.2 mm), round often beveled holes that are typically single and penetrate one valve of an articulated shell. The observed drilling frequency is comparable with frequencies observed in the Late Mesozoic and Cenozoic. The drilling organism displayed high valve and site selectivity, although the exact nature of the biotic interaction recorded by drill holes (parasitism vs. predation) cannot be established. In addition, prey/host size may have been an important factor in the selection of prey/host taxa by the predator/parasite. These results suggest that drilling interactions occasionally occurred at high (Cenozoic-like) frequencies in the Paleozoic. However, such anomalously high frequencies may have been restricted to small prey/host with small drill holes. Small drillings in C. cordata, and other Paleozoic brachiopods, may record a different guild of predators/parasites than the larger, but less common, drill holes previously documented for Paleozoic brachiopods, echinoderms, and mollusks.     

Drill Holes and Predation Traces versus Abrasion-Induced Artifacts Revealed by Tumbling Experiments

Drill holes made by predators in prey shells are widely considered to be the most unambiguous bodies of evidence of predator-prey interactions in the fossil record. However, recognition of traces of predatory origin from those formed by abiotic factors still waits for a rigorous evaluation as a prerequisite to ascertain predation intensity through geologic time and to test macroevolutionary patterns. New experimental data from tumbling various extant shells demonstrate that abrasion may leave holes strongly resembling the traces produced by drilling predators. They typically represent singular, circular to oval penetrations perpendicular to the shell surface. These data provide an alternative explanation to the drilling predation hypothesis for the origin of holes recorded in fossil shells. Although various non-morphological criteria (evaluation of holes for non-random distribution) and morphometric studies (quantification of the drill hole shape) have been employed to separate biological from abiotic traces, these are probably insufficient to exclude abrasion artifacts, consequently leading to overestimate predation intensity. As a result, from now on, we must adopt more rigorous criteria to appropriately distinguish abrasion artifacts from drill holes, such as microstructural identification of micro-rasping traces.     

Stereotypic and size-selective predation in Polinices pulchellus (Gastropoda: Naticidae) Risso 1826

Polinices pulchellus were size-selective in their choice of Cerastoderma edule. Large predators (12-15.9 mm shell length) selected both larger and a wider size range of cockles than smaller individuals (4-11.9 mm shell length). Considerable overlap occurred in the sizes of cockles frequently drilled by different size classes of snails, indicating that certain sizes of cockles may be most profitable to a wide range of predator sizes. Consumption rates were highest during July and August and were closely related to seawater temperature. Inner and outer drill hole diameters were both correlated with predator size, and the morphology of the drill hole was geometrically similar across a range of predator sizes. Polinices pulchellus showed no preference for either the left or right valve and drilled most cockles in the centre of the shell valve. The relationship between the distance of the drill hole from the umbo and prey size was unaffected by predator size, such that predators of different sizes were not found to drill cockles in different positions. When disturbed during drilling, incomplete drill holes were abandoned and, when drilling resumed, it occurred in new locations on the surface of the shell valve. The findings of this study highlight the stereotyped nature of drilling behaviour seen in the family Naticidae.     

Invasion of a naticid predator and associated changes in death assemblages of bivalve prey in northern Japan: implications for palaeoecological studies

The recent invasion of a naticid predator (Laguncula pulchella) and associated changes in the death assemblages of bivalve prey (Ruditapes philippinarum) provide a baseline for interpreting predator–prey interactions in the fossil record. This article presents quantitative data on size‐frequency distributions (SFDs) of living and death assemblages, prey size selectivity and drillhole site selectivity from the Tona Coast, northern Japan. Before the appearance of the predator, the SFD of the death assemblage exhibited a right‐skewed platykurtic distribution, and there were very few predatory drillholes. Once the predator appeared, frequencies of predatory drillholes increased, particularly in the smallest size class (2–10 mm shell length). Furthermore, juvenile peaks in the SFDs of death assemblages sharpened, and thus, SFDs exhibited strongly right‐skewed leptokurtic distributions. These changes suggest that intense naticid predation precluded juvenile clams from growing to adulthood, and thus, many dead shells of juvenile clams were introduced into the sediment. The changes in SFDs may also indicate intensification of predation pressure in the fossil record. No temporal shifts in prey size selectivity and drillhole site selectivity were noted, despite substantial changes in the demographics of Ruditapes philippinarum. This suggests that lack of specific size classes of preferred prey species is unlikely to be a primary factor accounting for size mismatches between predator and prey, because, in such situations, naticid predators probably attack other prey species. Therefore, such a factor is unlikely to primarily explain the less stereotypical predatory behaviour (i.e. low prey size selectivity and low drillhole site selectivity), which has been frequently recognized in fossil assemblages. Such less stereotypical predatory behaviour in fossil assemblages is likely to be explained by other factors, such as the existence of multiple predator taxa and lack of specific size classes of all available prey.     

Comparing predatory drillholes to taphonomic damage from simulated wave action on a modern gastropod

Marine drilling predation, in which the predator bores a hole through shelled invertebrate prey, plays a role in the structure of benthic communities. As drilling often leaves the prey shell otherwise undamaged, the resulting holes are also an excellent proxy for drilling predation pressure in the fossil record. Considering that a large number of predation studies focus on drilling predation in the fossil record, it is crucial that we are able to distinguish true drilling predation from taphonomy. The purpose of this study is to determine damage on Olivella biplicata shells, drilled by naticid gastropods, is distinguishable from taphonomically produced damage to these shells. In addition, the potential for preferential breakage due to either the presence or whether absence of a drillhole was investigated. Drilled and non-drilled O. biplicata shells were tumbled to simulate wave action and were checked at intervals to record accumulated damage. Drilled and non-drilled shells do not show a significant difference in damage accumulated while undergoing simulated wave action. Taphonomic damage is unlikely to be mistaken for drilling damage, due to the jagged, irregular appearance of taphonomically produced holes.     

Density‐dependent and ‐independent effects on the joint use of space by predators and prey in terrestrial arthropod food‐webs

The spatial distribution of predators and their prey is affected by their joint use of space. While the formation of such spatial patterns may be driven by density‐dependent and ‐independent factors our knowledge on the contribution of different land‐use activities on the formation of spatial patterns between predators and prey remains very limited. Agriculture is one of the most prevailing land‐use activities with strong effects on invertebrate densities and structural habitat conditions. Here, we used replicated conventionally and organically managed winter wheat fields to investigate the effects of agricultural land‐use on the spatial patterns of generalist predators and decomposer prey. We then identified the explanatory power of density‐dependent (prey and predator activity density) and density‐independent (vegetation structure) predictors for the observed spatial patterns. Generalist predators were regularly distributed only in conventionally managed fields and this pattern intensified with decreasing Collembola prey availability and increasing spider activity density. Segregation between carabid and spider predators was strongest in fields with lowest wheat plant height, suggesting more intense intraguild interactions in structurally less complex habitats. Collembola were aggregated independent of management and aggregation was strongest in fields with highest Collembola and carabid activity density. Spiders and Collembola prey were associated, but higher aphid densities under conventional management weakened or interrupted this spatial relationship. We conclude that active control of crop plant physiognomy by growth hormones and herbicides in conventionally managed fields promotes predator–predator segregation and that a high availability of aphid prey seems to decouple predator–Collembola prey associations. Our results emphasise the need for a more mechanistic understanding of the effects of land‐use on the formation of spatial patterns and species interactions, especially under scenarios of environmental change and an ongoing loss of biodiversity.     

Broken pieces: can variable ecological interactions be deduced from the remains of crab attacks on bivalve shells?

Shell fragmentation patterns that result from attacks by durophagous predators on hard‐shelled marine invertebrates are a rich source of indirect evidence that have proved useful in interpreting predation pressure in the fossil record and recent ecology. The behaviour and effectiveness of predators are known to be variable with respect to prey size. It is less well understood if variable predator–prey interactions are reflected in shell fragmentation patterns. Therefore, we conducted experimental trials to test the behavioural response of a living crab, Carcinus maenas, during successful predatory attacks on the blue mussel Mytilus edulis on two prey size categories. Further, we examined resultant shell fragments to determine whether specific attack behaviours by C. maenas could be successfully deduced from remaining mussel shells. In contrast to previous studies, we observed no significant differences in attack behaviour by the predators attributable to prey size. In most experimental predation events, crabs employed an ad hoc combination of five mechanisms of predation previously described for this species. We identified seven categories of shell breakage in predated mussels, but none of these were unambiguously correlated with specific attack behaviour. Combined attack behaviours may produce shell breakage patterns that have previously been assumed to be attributable to a single behaviour. While specific patterns of shell breakage are clearly attributable to durophagy, the results of this study provide important insights into the limitations of indirect evidence to interpret ecological interactions.     

Evidence of weaker phenotypic plasticity by prey to novel cues from non‐native predators

A central question in evolutionary biology is how coevolutionary history between predator and prey influences their interactions. Contemporary global change and range expansion of exotic organisms impose a great challenge for prey species, which are increasingly exposed to invading non‐native predators, with which they share no evolutionary history. Here, we complete a comprehensive survey of empirical studies of coevolved and naive predator?prey interactions to assess whether a shared evolutionary history with predators influences the magnitude of predator‐induced defenses mounted by prey. Using marine bivalves and gastropods as model prey, we found that coevolved prey and predator‐naive prey showed large discrepancies in magnitude of predator‐induced phenotypic plasticity. Although naive prey, predominantly among bivalve species, did exhibit some level of plasticity – prey exposed to native predators showed significantly larger amounts of phenotypic plasticity. We discuss these results and the implications they may have for native communities and ecosystems.     

Geometric factors influencing the diet of vertebrate predators in marine and terrestrial environments

Predator–prey relationships are vital to ecosystem function and there is a need for greater predictive understanding of these interactions. We develop a geometric foraging model predicting minimum prey size scaling in marine and terrestrial vertebrate predators taking into account habitat dimensionality and biological traits. Our model predicts positive predator–prey size relationships on land but negative relationships in the sea. To test the model, we compiled data on diets of 794 predators (mammals, snakes, sharks and rays). Consistent with predictions, both terrestrial endotherm and ectotherm predators have significantly positive predator–prey size relationships. Marine predators, however, exhibit greater variation. Some of the largest predators specialise on small invertebrates while others are large vertebrate specialists. Prey–predator mass ratios were generally higher for ectothermic than endothermic predators, although dietary patterns were similar. Model‐based simulations of predator–prey relationships were consistent with observed relationships, suggesting that our approach provides insights into both trends and diversity in predator–prey interactions.     

Reappraising the early evidence of durophagy and drilling predation in the fossil record: implications for escalation and the Cambrian Explosion

The Cambrian Explosion is arguably the most extreme example of a biological radiation preserved in the fossil record, and studies of Cambrian Lagerstätten have facilitated the exploration of many facets of this key evolutionary event. As predation was a major ecological driver behind the Explosion – particularly the radiation of biomineralising metazoans – the evidence for shell crushing (durophagy), drilling and puncturing predation in the Cambrian (and possibly the Ediacaran) is considered. Examples of durophagous predation on biomineralised taxa other than trilobites are apparently rare, reflecting predator preference, taphonomic and sampling biases, or simply lack of documentation. The oldest known example of durophagy is shell damage on the problematic taxon Mobergella holsti from the early Cambrian (possibly Terreneuvian) of Sweden. Using functional morphology to identify (or perhaps misidentify) durophagous predators is discussed, with emphasis on the toolkit used by Cambrian arthropods, specifically the radiodontan oral cone and the frontal and gnathobasic appendages of various taxa. Records of drill holes and possible puncture holes in Cambrian shells are mostly on brachiopods, but the lack of prey diversity may represent either a true biological signal or a result of various biases. The oldest drilled Cambrian shells occur in a variety of Terreneuvian‐aged taxa, but specimens of the ubiquitous Ediacaran shelly fossil Cloudina also show putative drilling traces. Knowledge on Cambrian shell drillers is sorely lacking and there is little evidence or consensus concerning the taxonomic groups that made the holes, which often leads to the suggestion of an unknown ‘soft bodied driller’. Useful methodologies for deciphering the identities and capabilities of shell drillers are outlined. Evidence for puncture holes in Cambrian shelly taxa is rare. Such holes are more jagged than drill holes and possibly made by a Cambrian ‘puncher’. The Cambrian arthropod Yohoia may have used its frontal appendages in a jack‐knifing manner, similar to Recent stomatopod crustaceans, to strike and puncture shells rapidly. Finally, Cambrian durophagous and shell‐drilling predation is considered in the context of escalation – an evolutionary process that, amongst other scenarios, involves predators (and other ‘enemies’) as the predominant agents of natural selection. The rapid increase in diversity and abundance of biomineralised shells during the early Cambrian is often attributed to escalation: enemies placed selective pressure on prey, forcing phenotypic responses in prey and, by extension, in predator groups over time. Unfortunately, few case studies illustrate long‐term patterns in shelly fossil morphologies that may reflect the influence of predation throughout the Cambrian. More studies on phenotypic change in hard‐shelled lineages are needed to convincingly illustrate escalation and the responses of prey during the Cambrian.     

Additive effects of predator diversity on pest control caused by few interactions among predator species

1. Studies of the impact of predator diversity on biological pest control have shown idiosyncratic results. This is often assumed to be as a result of differences among systems in the importance of predator–predator interactions such as facilitation and intraguild predation. The frequency of such interactions may be altered by prey availability and structural complexity. A direct assessment of interactions among predators is needed for a better understanding of the mechanisms affecting prey abundance by complex predator communities. 2. In a field cage experiment, the effect of increased predator diversity (single species vs. three‐species assemblage) and the presence of weeds (providing structural complexity) on the biological control of cereal aphids were tested and the mechanisms involved were investigated using molecular gut content analysis. 3. The impact of the three‐predator species assemblages of aphid populations was found to be similar to those of the single‐predator species treatments, and the presence or absence of weeds did not alter the patterns observed. This suggests that both predator facilitation and intraguild predation were absent or weak in this system, or that these interactions had counteracting effects on prey suppression. Molecular gut content analysis of predators provided little evidence for the latter hypothesis: predator facilitation was not detected and intraguild predation occurred at a low frequency. 4. The present study suggests additive effects of predators and, therefore, that predator diversity per se neither strengthens nor weakens the biological control of aphids in this system.     

Predator–prey interactions and metabolic rates are altered in stable and unstable groups in a social fish

Understanding the determinants and consequences of predation effort, success and prey responses is important since these factors affect the fitness of predators and prey. When predators are also invasive species, the impacts on prey can be particularly far-reaching with ultimate ecosystem-level consequences. However, predators are typically viewed as behaviourally fixed within this interaction and it is unclear how variation in predator social dynamics affects predator–prey interactions. Using the invasive eastern mosquitofish Gambusia holbrooki and a native glass shrimp Paratya australiensis in Australia, we investigated how varying levels of social conflict within predator groups influences predator–prey interactions. By experimentally manipulating group stability of G. holbrooki, we show that rates of social conflict were lower in groups with large size differences, but that routine metabolic rates were higher in groups with large size differences. Predation effort and success did not vary depending on group stability, but in stable groups predation effort by aggressive dominants was greater than subordinates. The anti-predator responses of prey to the stability of predator groups were mixed. While more prey utilized shelters when exposed to stable compared to unstable groups of predators, a greater proportion were sedentary when predator groups were unstable. Overall, this study demonstrates predator group stability is modulated by differences in body size and can influence prey responses. Further, it reveals a hidden metabolic cost of living in stable groups despite reduced overt social conflict. For invasive species management, it is therefore important to consider the behavioural and physiological plasticity of the invasive predators, whose complex social interactions and metabolic demands can modulate patterns of predator–prey interactions.     

Drilling predation on serpulid polychaetes (Ditrupa arietina) from the pliocene of the Cope Basin, Murcia Region, Southeastern Spain

We report quantitative analyses of drilling predation on the free-living, tube-dwelling serpulid polychaete Ditrupa arietina from the Cope Cabo marine succession (Pliocene, Spain). Tubes of D. arietina are abundant in the sampled units: 9 bulk samples from 5 horizons yielded ~5925 specimens of D. arietina. Except for fragmentation, tubes were well preserved. Complete specimens ranged from 3.1 to 13.4 mm in length and displayed allometric growth patterns, with larger specimens being relatively slimmer. Drilled Ditrupa tubes were observed in all samples. Drillholes, identified as Oichnus paraboloides, were characterized by circular to elliptical outline (drillhole eccentricity increased with its diameter), parabolic vertical profile, outer diameter larger than inner diameter, penetration of one tube wall only, narrow range of drill-hole sizes, and non-random (anterior) distribution of drillholes. A total of 233 drilled specimens were identified, with drilling frequencies varying across horizons from 2.7% to 21% (3.9% for pooled data). Many tube fragments were broken across a drillhole suggesting that the reported frequencies are conservative and that biologically-facilitated (drill-hole induced) fragmentation hampers fossil preservation of complete serpulid tubes. No failed or repaired holes were observed. Multiple complete drillholes were present (3.9%). Drilled specimens were significantly smaller than undrilled specimens and tube length and drill-hole diameter were weakly correlated. The results suggest that drillholes were produced by a size-selective, site-stereotypic predatory organism of unknown affinity. The qualitative and quantitative patterns reported here are mostly consistent with previous reports on recent and fossil Ditrupa and reveal parallels with drilling patterns documented for scaphopod mollusks, a group that is ecologically and morphologically similar to Ditrupa. Consistent with previous studies, the results suggest that free-dwelling serpulid polychaetes are preyed upon by drilling predators and may provide a viable source of data on biotic interactions in the fossil record.     

Predator control of ecosystem nutrient dynamics

Predators are predominantly valued for their ability to control prey, as indicators of high levels of biodiversity and as tourism attractions. This view, however, is incomplete because it does not acknowledge that predators may play a significant role in the delivery of critical life‐support services such as ecosystem nutrient cycling. New research is beginning to show that predator effects on nutrient cycling are ubiquitous. These effects emerge from direct nutrient excretion, egestion or translocation within and across ecosystem boundaries after prey consumption, and from indirect effects mediated by predator interactions with prey. Depending on their behavioural ecology, predators can create heterogeneous or homogeneous nutrient distributions across natural landscapes. Because predator species are disproportionately vulnerable to elimination from ecosystems, we stand to lose much more from their disappearance than their simple charismatic attractiveness.     

Clumping behavior as a strategy against drilling predation: Implications for the fossil record

Drilling gastropod predators are of particular interest to paleontologists, because predatory drill-holes in marine invertebrates serve as one of the rare sources of data for the study of ancient predator-prey interactions. Modern laboratory studies are an important part of predation research providing valuable ecological insight and constraining fossil evidence and interpretations. Previous studies have shown that mussels use clumping behavior against durophagous predation [Okamura, B., 1986. Group living and the effects of spatial position in aggregations of Mylitus edulis. Oecologia 69, 341-347.; Lin, J., 1991. Predator-prey interactions between blue crabs and ribbed mussels living in clumps. Estuar. Coast. Shelf Sci. 32, 61-69.], but its role against drilling predation had not been explored. In this study, we explore the effect of clumping on predator success (drill-hole frequency) and prey handling (drill-hole position) using the mussel, Mytilus trossulus, as prey and the gastropod, Nucella lamellosa, as drilling predator. We assigned mussels to two groups: in one, mussels were allowed to clump together with their byssal threads, and in the other, they were kept separate. We observed a significant decrease in the drilling frequency within the group containing clumped mussels, confirming that clumping acts as a successful anti-predatory strategy against drilling predators. The use of clumping as an effective strategy against multiple types of predators may relax the trade-offs associated with aggregated lifestyles [Bertness, M.D., Grosholz, E., 1985. Population dynamics of the ribbed mussel, Geukensia demissa: the costs and benefits of an aggregated distribution. Oecologia 67, 192-204.]. The increased benefit and unchanged metabolic cost of clumped living alters estimates of individual fitness with evolutionarily significant implications (e.g., eliminating the need to invoke group or species selection to explain the adaptive benefit of an aggregated lifestyle). In spite of potential differences in prey handling and grappling due to clumping, mean drill-hole placement and variation in drill-hole placement showed no significant differences between the two groups. These observations suggest that comparison of predation intensities across clumping and non-clumping taxa must consider the anti-predatory effect of this behavior.     

Naticid gastropod predation in the Gatun Formation (late Middle Miocene), Panama: preliminary assessment

Understanding predator-prey interactions is an important component of community studies, both present and past. Patterns of naticid predation in a fossil molluscan assemblage were studied by examination of drilling frequencies in a series of samples collected at three sites of the Gatun Formation (late Middle Miocene), Panama. Overall drilling intensities were relatively low (18 %) and were not correlated with abundance. Turritellids, turrids, and terebrids (making up to 11 % of the studied fauna) were the most consumed, representing almost 29 % of the total prey. Especially important were turritellids representing over 20 % of the total consumed prey. Albeit abundant (54 % of the studied fauna), columbellids, cerithiids, and marginellids showed low drilling intensities (8.2–10.4 %). Naticids were the major predators. Con-familial drilling among naticids is high and did not seem to be related to absence of preferred prey. Consistent with other studies, these data indicate that predators demonstrate high prey selectivity.