Effectiveness of micromorphy against drilling predation: Insights from early Miocene faunal assemblage of Quilon limestone, India

The nature of drilling predation, although well documented for molluscan fossils, is understudied for micromolluscs (<5mm). Studying predation in micromolluscs is especially critical in evaluating the adaptive significance of micromorphy against predation and assessing the importance of predator-prey size relationship (PPSR). This study documents drilling predation event in microbivalves from early Miocene (Burdigalian) fossil assemblage of Quilon limestone from Kerala, India. Our sample of ∼2000 valves represent nine families with an average drilling frequency (DF) of 0.06 and an incomplete drilling frequency (IDF) of 0.26. The characteristic drillhole morphology and occurrence of five genera of modern drilling gastropods (Naticid: Natica, Tanea and Polinices; Muricid: Triplex and Dermomurex) from the same locality reveals the predator identity. Predation in the studied assemblage is found to be highly selective in terms of prey taxa, size, mobility and site selection. Six out of nine families show evidence of predation indicating taxon selectivity. Poor correlation between DF and abundance further supports this view. Failed attacks are strongly correlated with morphological features such as surface ornamentation (Lucinidae), presence of conchiolin layers (Corbulidae). Drilling occurs primarily on medium size class and prey outside this size range show lower rate of attack. This indicates the existence of an “inverse size refugia” for extremely small prey along with the classical size refugia existing for large prey. Mobility is found to be a deterrent to drilling predation and it also increases failure. Microbenthos of Quilon limestone shows a lower predation intensity in comparison to the Miocene macrobenthos worldwide including coeval formation of the Kutch Basin. The interaction in microbenthos is more strongly size-dependent in contrast to the Kutch fauna. Reduced predation intensity in microfauna and existence of “inverse size refugia” support the claim of micromorphy acting as a defense mechanism and highlights the role of size-dependent predation in marine benthos.


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Predation is considered as one of the primary ecological processes that drives natural  It has long been recognized that predators are generally larger than their prey [17, but 60 see 18], especially in highly size-structured marine ecosystem [19][20][21]. Size selectivity is 61 largely true for drilling predator-prey system [22][23][24] with some exceptions [25]. The prey 62 selection by a drilling predator is a balance between invested energy (through foraging, 63 drilling and consumption) and energy gain (dependent on prey size) [22,26]. As predator size 64 increases, metabolic demand becomes more resulting in an increase in the rate of food intake 65 to match the energetic demands [27]. Such increase in energy requirement can be tackled by 66 choosing either a larger prey or attacking multiple smaller preys; the decision depends on the 67 availability and distribution of prey-size in a community [28]. Prey often develops anti- 68 predatory strategies as a response to an increase in predation pressure. Increase in effective 69 size and attaining a "size refugia" is one of the common anti-predatory strategies exploited by 70 marine invertebrates [29][30][31][32][33]. Such "size refugia" is often a result of handling limit of the 71 predator [22]. Interestingly, prey smaller than the "size refugia" are not always attacked with 72 equal frequency. It has been observed that the medium size class are often attacked the most, 73 making them the preferred size class for predation [13,25]. This points to an apparent 74 predation-resistance of extremely small sized prey. If the attacks on extremely small prey 75 significantly reduces the net energy gain of the predator, it would be expected to find a low 76 predation pressure in smaller sized prey [27]. This may lead to an "inverse size refugia" in 77 the smaller size class and shield the extremely small prey from predation. Harper and Peck 78 [34] also demonstrated low intensity of durophagous predation in tropical brachiopods and 79 attributed the micromorphic nature of tropical brachiopods as a defense against durophagous 80 predation. Unfortunately, the drilling predation dynamics in juveniles and extremely small 81 molluscan prey are rarely studied and hence, not well understood to test the existence of 82 predation resistance in smaller prey.

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The Quilon limestone of early Miocene, exposed in southern state of Kerala, India   Bulk sample of loose sediments (~230gm) were soaked for 2-3 days in normal water.

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Repeated heating and thawing was used to separate specimens from the limestone matrix.

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The processed samples were then sieved using a stacked sieve of five mesh sizes ( (Fig 2, Fig 3A). A total of 62 valves show drillholes representing six families; Arcidae,

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Majority of the drillholes are located in the middle (71%), followed by edge drilling 190 (18%) and umbonal drilling (11%) ( Table 1). Except for Anomidae and Glycymerididae, all 191 the families show rarity of umbonal and edge drilling ( Fig 3D).  Table 2). Naticid drillings are significantly higher in mobile families 201 and Muricids drillings in immobile families (Table 2).  Size selectivity 211 We found a significant difference in size distribution between groups with and 212 without drilling (complete and incomplete) ( Table 5). The inferred size of the Muricids is significantly larger than that of the 249 Naticids.  The DF and IDF of the microscopic bivalves are significantly lower than those of 262 larger bivalves of Kutch (Fig 9A, B, Table 6). The site selectivity between two provinces 263 were also compared ( Fig 9C, Table 6). In comparison to Kutch, the umbonal proportion of    Fig 10A). Moreover, it does not show a significant 277 correlation between size of prey and Naticid predator -a trend that is observed in microfauna 278 of Kerala (Fig 10B, Table 5). Both the regions, however, show significant negative 279 correlation between predator size with prey/predator ratio (Fig 10C, Table 5). When we 280 compared the data with three models of increasing, decreasing and constant prey size with value of DF for corresponding family (Fig 11).

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Previous studies reported the existence of a handling limit for a specific predator, 420 beyond which the attacks are likely to fail and prey larger than this handing limit is immuned  trend either ( Fig.2A, [90]). However, it is known that the preservation potential of small