Record of Naticid Predation on Scaphopods (Mollusca) from the Latest Maastrichtian of Rajahmundry,India

Drilling predation provides a rare opportunity to study and quantify prey-predator interactions in the fossil record. Records of drilling predation on scaphopod mollusc are rare. Here, we report naticid drilling predation on scaphopods from a “Turritelline-dominated assemblage” (TDA) stratigraphically just below the K-Pg boundary sections in Rajahmundry, India, which was situated in the Southern Hemisphere during that time. Low drilling frequency was found in the present assemblage based on 248 specimens, which was similar to most of the Cretaceous values previously reported. Majority of the specimens of previous studies were reported from higher latitudes in the Northern Hemisphere. Our report extended the palaeobiogeography of naticid predation on scaphopods into the Southern Hemisphere. Size and site stereotypy of drillholes on the scaphopod shell suggested that predatory behavior of naticids was already highly evolved, but evidence of escalation was less clear in scaphopod prey.     

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.     

Drilling and crushing predation on scaphopods from the Miocene of the Netherlands

Klompmaker, A.A. 2011: Drilling and crushing predation on scaphopods from the Miocene of the Netherlands. Lethaia, Vol. 44, pp. 429–439. Reports on the predators of scaphopods are rare. This study records two types of predation traces on the Miocene dentaliid scaphopod Fissidentalium sp. from Langenboom in the Netherlands. The first type is demonstrated by naticid drillholes, located primarily on the middle (and thickest) part of the shell. Based on the examination of more than 700 specimens, the percentage of completely drilled scaphopods is low, at 1%. This is in line with the first graphical overview of drilling percentages on scaphopods through time. The second type of predation is found as jagged, arcuate margins at the functionally anterior end of a significant part of the scaphopod population. These breakages were not caused by pressure due to overburden, as experimental results indicate that such breakages form at right angles to the longitudinal axis of the shell. Reworking was also ruled out, mainly because the breakages were formed at the anterior end of the shell only. Rather, the damage is attributed to carnivorous decapods chipping/peeling with their claws or mandibles. The predation traces suggest that Fissidentalium sp. was a shallow burrower. □Scaphopoda, drillholes, predators, Miocene, the Netherlands, Langenboom     

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.     

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.     

Drilling predation on the clypeasteroid echinoid Echinocyamus pusillus from the Mediterranean Sea (Giglio,Italy)

Drilling predation of cassid gastropods (tonnacean) on echinoids is common in marine environments but is rarely documented. Tests of the minute clypeasteroid Echinocyamus pusillus OF Müller (1776) were collected from the Mediterranean Sea (Isola del Giglio, Italy). Besides general morphology, features pertaining to the morphology and distribution of predatory boreholes were examined. Furthermore, borehole frequencies among different samples sites were compared. Cassid gastropods are assumed to be the originators of the boreholes. A total of 1061 tests were analysed for drilling rates with 15.3% drilled with predominantly single boreholes. The borehole morphology is strongly affected by the microstructure of the skeleton; the borehole outline is irregular if drilled within areas where ambulacral pores are present. Vertical borehole morphology is influenced by stereom density. The size frequencies of non-drilled and drilled specimens show significant differences. Comparisons of borehole size with test size show only a low correlation between predator and prey size. The distribution of boreholes shows a high site selectivity of the predator for the aboral side of the test and the petalodium.     

Evolutionary trends within bivalve prey of chesapeake group naticid gastropods

Five genera of Miocene bivalves evolved antipredatory adaptations in response to predation by drilling naticid gastropods. I examined the evolution of two traits affecting predator‐prey interaction, prey shell thickness (TH) and internal volume (IV). Thickness controls predation costs by determining drilling time, and internal volume influences the benefit derived by the predator.

Internal volume showed no consistent pattern of temporal change among the taxa studied. IV fluctuated nondirectionally during the history of most genera, though both increasing and decreasing trends occurred within species ofAstarte. In contrast, all five genera exhibited significant thickness increases (from 8–157%) during the three‐million‐year interval. Both gradual intraspecific and interspecific directional changes occurred. Taxa with the greatest predation intensities displayed the most change, suggesting that predation selected for the thickness increases. Increased thickness apparently reduced predation; a significant negative correlation between TH and predation intensity occurred within four of the bivalve genera. Improvement of predator capabilities apparently did not keep pace with increased antipredatory morphologic adaptations over the interval studied.     

Traces of Naticid Predation on the Gryphaeid Oyster Pycnodonte dissimilaris: Epifaunal Drilling of Prey in the Paleocene

Traces of drilling predation by naticid gastropods were observed on 51 valves of the free-lying, semi-infaunal oyster Pycnodonte dissimilaris (Gryphaeidae) from the Paleocene Hornerstown Formation, in New Jersey. Stereotypic behavior of the predator is indicated by the highly constrained placement of drill holes, 94% of which are centrally located on the oyster shells. Predator—prey mismatches in size, involving small predators that drilled through the upper valves of relatively large oysters, are documented by comparison of outer borehole diameter, as an index of predator size, with the sizes of the oyster shells. Results of this analysis suggest that at least some prey were drilled epifaunally, as they were too large to be manipulated and buried by the predator. This indicates, together with reports of epifaunal drilling by living naticids, that such behavior is geographically and stratigraphically more widespread in the Naticidae than has previously been acknowledged. This in turn suggests that epifaunal drilling of prey is a plesiomorphic, opportunistic mode of behavior, conserved in the evolution of the Naticidae, that has permitted subsequent escalation or expansion in range of naticid foraging from a more narrowly defined infaunal paradigm into exposed intertidal refugia.     

Body size variation in the sexually dimorphic scaphopod Rhabdus rectius (Carpenter, 1864) (Dentaliida: Rhabdidae)

ABSTRACT

Male-biased sexual size dimorphism typically evolves via sexual selection for larger males that are favoured by choosy females or are more successful in mate competition with other males. Among marine invertebrates that broadcast their gametes into the ocean for fertilisation, this form of sexual size dimorphism is rare because such species lack direct interactions among males or between the sexes. However, the broadcast-spawning tusk shell Rhabdus rectius was recently reported to show strong male-biased sexual size dimorphism. That pattern might imply interesting and undiscovered sexual selection in this species. We found instead that the distribution of body size variation (weight, shell length) was similar between males and females of R. rectius, and mean sizes were not different between the sexes. However, we noted a male-biased sex ratio (～1:1.3) in our large sample of individuals. Many live scaphopods (and several dead shells) showed partial or complete boreholes drilled by predatory gastropods. Boreholes were observed on males and females in similar proportions. We collected scaphopods along with multiple individuals of one likely scaphopod predator, the small moon snail Euspira pallida, and in the lab we observed successful attacks by moon snails on tusk shells.     

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.     

Predation in a temporary pond with special attention to the trophic role of Triops cancriformis (Crustacea: Branchiopoda: Notostraca)

Temporary ponds are described as environments with a low predation pressure. Notostracans inhabit these types of ponds, and some populations acquire a high proportion of larger individuals, whose feeding behaviour is mainly predatory. The predation nature of Triops cancriformis is not widely accepted, because its diet is still partly controversial. We analysed the diet of one population of T. cancriformis in a Mediterranean temporary pond (Espolla pond, NE Iberian peninsula) to evaluate its predation behaviour. The gut content of the individuals bigger than 10 mm is mainly composed of detritus, plant fibres and microcrustaceans (cladocerans, ostracods and copepods). The prey number increases with the body size of individual T. cancriformis as previously described. Sex-biased predation was observed for one copepod prey, but not for the other. Predation pressure in that community was monitored along six hydroperiods as the percentage of predator biomass (not only T. cancriformis) in relation to the non-predator biomass. The proportion of predator biomass is high, and this contrasts with the low predation pressure expected for a temporary system with short hydroperiods.     

Invasion success in communities with reciprocal intraguild predation depends on the stage structure of the resident population

The probability of individuals being targeted as prey often decreases as they grow in size. Such size‐dependent predation risk is very common in systems with intraguild predation (IGP), i.e. when predatory species interact through predation and competition. Theory on IGP predicts that community composition depends on productivity. When recently testing this prediction using a terrestrial experimental system consisting of two phytoseiid mite species, Iphiseius degenerans as the IG‐predator and Neoseiulus cucumeris as the IG‐prey, and pollen (Typha latifolia) as the shared resource, we could not find the predicted community shift. Instead, we observed that IG‐prey excluded IG‐predators when the initial IG‐prey/IG‐predator ratio was high, whereas the opposite held when the initial ratio was low, which is also not predicted by theory. We therefore hypothesized that the existence of vulnerable and invulnerable stages in the two populations could be an important driver of the community composition. To test this, we first demonstrate that IG‐prey adults indeed attacked IG‐predator juveniles in the presence of the shared resource. Second, we show that the invasion capacity of IG‐predators at high productivity levels indeed depended on the structure of resident IG‐prey populations. Third, we further confirmed our hypothesis by mimicking successive invasion events of IG‐predators into an established population of IG‐prey at high productivity levels, which consistently failed. Our results show that the interplay between stage structure of populations and reciprocal intraguild predation is decisive at determining the species composition of communities with intraguild predation.     

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.     

Macroecology and evolution of a crab ‘super predator’, Menippe mercenaria (Menippidae), and its gastropod prey

It is widely accepted that the fossil record shows both the evolution of more powerful durophagous marine predators through time and, in response, major shifts in life mode and morphology for many prey taxa. Few fossil studies, however, have successfully identified particular predator species with respect to causing evolutionary change in particular prey species. We present evidence that the evolutionary appearance in the western Atlantic of the stone crab, Menippe mercenaria, an extraordinarily powerful durophagous predator, contributed to the appearance of sinistrality, which is very rare, in two genera of marine gastropods (Conus and Sinistrofulgur) during the Pliocene. Based on this conclusion, we suggest that modern fishing pressure on stone crabs may lead to evolutionary changes in their present day prey.     

Predation at a snail's pace: what's time to a gastropod?

Summary Predation by naticid gastropods shows evidence of adaptation to maximize the rate of energy intake. The predation rate of Polinices duplicatus feeding on artificially altered, thin-shelled Mercenaria mercenaria was faster than the predation rate on normal Mercenaria. The rate of energy intake was limited by handling time. The time saved by predation on thin-shelled prey was used to forage. Thus time was shown to be valuable to P. duplicatus, and cost-benefit functions using time and energy as currencies are appropriate for estimating dietary efficiency and predicting prey choice.Despite the clear superiority of thin-shelled prey, P. duplicatus did not learn to prefer this novel prey type, suggesting that predator choices are sterotyped, reflecting optima selected over evolutionary time.     

Effect of durophagy on drilling predation: a case study of Cenozoic molluscs from North America

Drilling predation represents one of the most widely studied biotic interactions preserved in the fossil record, and complete and incomplete drill holes have been commonly used to explore spatial and temporal patterns of this phenomenon. While such patterns are generally viewed solely in terms of the interactions between predator and prey, they might also be affected by extrinsic ecological factors. Recent experiments have demonstrated that in the presence of a secondary predator (crab), the incomplete drilling frequency increases indicating increasing abandonment of the prey, and drilling frequency decreases implying a decrease in successful attacks. Here, we tested whether the effect of secondary predators on drilling frequencies can be detected in the fossil record. Using fossil molluscs from six Plio-Pleistocene localities, we found that repair scar frequencies, a proxy for activity of durophagous predators, correlate directly with incomplete drill hole frequencies and inversely with complete drill hole frequencies. These results suggest that the activity and success of drilling predators is influenced not just by the prey, but also by secondary predators.     

Predation on freshwater snails in Miocene Lake Steinheim: a trigger for intralacustrine evolution?

Shells of the freshwater gastropods Gyraulus trochiformis (Planorbidae or ramshorn snails) and Bania pseudoglobula (formerly Pseudamnicola, Hydrobiidae) from Miocene Steinheim Basin in SW Germany contain small holes with a mean diameter of 0.8 mm. Analyses of comparable holes are so far unknown from fossil or extant assemblages of freshwater shells. This analysis of the perforated shells suggests that the holes were not formed by post‐depositional or pure taphonomic processes. Instead, they were most likely produced by predators. This analysis widens the means for identification of predation on freshwater snail shells that can be used in other palaeolimnological studies. The co‐occurrence of fish teeth and perforated shells in the studied samples as well as the perforation features suggest that the predator was either barbel or tench fish. The correlation between shell sizes and hole diameters suggests a size relationship between predator and prey that may generally be related to gape‐limited fish predators. The co‐occurrence of perforated shells in these lake sediments with a dominance of large and armoured shells suggest that these larger shells with protuberances and knobs could not be crushed by the gape‐limited fish predators. This analysis is the basis for a hypothesis that the endemic evolution of Gyraulus in Lake Steinheim, with some varied forms of shell thickness and morphology, was triggered by a predator–prey relationship based on adaptations to avoid shell‐breaking predators.     

Environmental variation and the predator-specific responses of tropical stream insects: effects of temperature and predation on survival and development of Australian Chironomidae (Diptera)

The threat posed by predation varies among predator species and with environmental context, and prey species often adjust their responses accordingly. We investigated such effects within an insect assemblage from a tropical Australian stream. These systems are frequently subjected to catastrophic floods, often suggested to reduce the importance of predation in streams, and invertebrate faunas are characterised by relatively broad environmental tolerances. Impacts of the hunting predator Australopelopia prionoptera (Diptera: Chironomidae) and an undescribed ambush predator from the Polycentropodidae (Trichoptera) on survival and development of two species of tubicolous Chironomidae, Echinocladius martini (Orthocladiinae) and Polypedilum australotropicus (Chironominae), were assessed in laboratory microcosms. A further experiment investigated how impacts of Australopelopia varied over a broad range of temperatures, exceeding that experienced annually by the studied populations. Neither predator impacted survivorship for E. martini, but the presence of the polycentropodid caused E. martini to spend longer as larvae and reduced adult longevity, and adult females were smaller-sized and had smaller oocytes. In contrast, both predators reduced survivorship of P. australotropicus, but only Australopelopia affected its development, causing reductions in pupal duration and oocyte size. The observed non-lethal impacts of predation reflect the threat each predator is known to pose to each prey species in situ. Impacts of predation varied little with temperature, reflecting the broad thermal tolerances of all study species. The predator-specific responses of the prey species imply that predation is a significant selective force in tropical Australian streams, although fluctuation in intensity of predation associated with flooding may limit its importance for community structure and prey diversity at larger scales. Our results indicate a more limited scope for environmental modification of predator–prey relationships in faunas characterised by broad physiological tolerances.     

Processes affecting newly-settled juveniles and the consequences to subsequent community development

Summary

Processes affecting the growth and mortality of the juvenile benthic life-stages that immediately follow larval metamorphosis and settlement are as important as those processes controlling the supply of settling larvae or later interactions among established adults. In addition, the ecology of juveniles is of ten distinctly different from that of other life-stages, including differences in interactions with predators and competitors and responses to the physical environment. In particular, newly-settled stages of ten experience quantitatively or qualitatively different predation than older life-stages. We have documented this in a New England hard substrate community where the wrasse, Tautogolabrus adspersus, and two species of tiny gastropods, Mitrella lunata and Anachis lafresnayi, prey on newly-settled andjuvenile ascidians but not on adults. An extensive series of field experiments was conducted using artificial pilings placed subtidally. Results demonstrated that (1) the predators were extremely active and fairly specific in their prey, (2) predators could eliminate prey species regardless of settlement densities, (3) predation varied drastically with life-stage, and (4) predators control community structure and composition by altering the number of settling larvae that survived their first several weeks to become identifiable recruits. Because of differences in predator abundances the development and species dominance within the community varied drastically between sites.