- Email: [email protected]
Boring predation and Mesozoic articulate brachiopods
Palaeogeography, Palaeoclimatology, Palaeoecology 158 (2000) 15–24 www.elsevier.nl/locate/palaeo
Boring predation and Mesozoic articulate brachiopods E.M. Harper *, D.S. Wharton 1 Department of Earth Sciences, Downing Street, Cambridge CB2 3EQ, UK Received 8 June 1999; accepted for publication 28 October 1999
Abstract A systematic survey of all the Mesozoic brachiopods in the large collections of the Sedgwick Museum (Cambridge University) has revealed more than 213 predatory boreholes from a wide range of largely British localities. It seems likely that this type of predation was not infrequent, at least locally, as evidenced by the proportion of bored valves at some localities and the degree of stereotypy shown in borehole positioning. The size of the boreholes and their neat circular cross sections suggest that they were made by large, epifaunal predators using chemical attack and those of post-Albian age may be comfortably (if not confidentally) assigned to muricid gastropods. Although it is likely that bivalves, with their greater flesh yields, were the preferred prey item in most Mesozoic shelly benthic communities, it is apparent that boring predators may have resulted in a significant predation pressure on articulate brachiopods. © 2000 Elsevier Science B.V. All rights reserved. Keywords: brachiopods; gastropods; Mesozoic; predation
1. Introduction There is a strange contradiction in the perceived importance of predation pressure on the evolution of brachiopods. On the one hand, there is a popular notion that brachiopods, articulates in particular, are unattractive to predators and have been so in the geological past (Rudwick, 1970; Thayer, 1981, 1985; Thayer and Allmon, 1990), in which case predation cannot have been an important evolutionary selection pressure. On the other hand, however, direct predation pressure on vulnerable brachiopod taxa has been used to explain why brachiopods failed to significantly re-radiate after the Permian–Triassic mass extinction (e.g. Stanley, 1974, 1977, 1979; Donovan and Gale, * Corresponding author. Fax: +44-1223-333450. E-mail address: [email protected] ( E.M. Harper) 1 Current address: Department of Geology, University of Bristol, Queen’s Road, Bristol BS8 1JR, UK.
1990), whilst Vermeij (1983) has pointed to the potential vulnerability of the bi-valved form. The supposition that brachiopods are not (and have not been) important prey items is based on two major lines of evidence. Firstly, there are few published accounts of predation on modern brachiopods and secondly, the experimental observation by Thayer (1985) that a range of modern predators appeared to prefer bivalve mussels to brachiopods. Several suggestions have advanced for this apparent lack of predation pressure: 1. their low body mass, up to 50% of which is not readily accessible in punctate taxa (Curry and Ansell, 1986) which makes them unattractive in comparison to bivalves with their greater yield; and 2. a lack of palatability due to spicules within the flesh and the possibility that their tissues may contain toxins ( Thayer, 1985; Thayer and Allmon, 1990).
0031-0182/00/$ - see front matter © 2000 Elsevier Science B.V. All rights reserved. PII: S0 0 3 1 -0 1 8 2 ( 9 9 ) 0 0 16 4 - 9
16
E.M. Harper, D.S. Wharton / Palaeogeography, Palaeoclimatology, Palaeoecology 158 (2000) 15–24
It should be noted, however, that to date no toxins have been isolated from brachiopod tissue (Peck, 1993). Nevertheless, there are records of predation on Recent articulate brachiopods by a range of modern predators, for example, fish ( Witman and Cooper, 1983), asteroids (Mauzey et al., 1968) and gastropods (Noble and Logan, 1981; Witman and Cooper, 1983). It is difficult to believe that ancient brachiopods did not suffer similar predation, particularly during the Palaeozoic and Mesozoic when they formed an important part of the shelly benthos. However, reports of predated fossil articulates are relatively few and most are based on Palaeozoic material. The victims of many predatory methods may not always be readily identified in the fossil record; for example it is difficult to distinguish damage inflicted by crushing predators from taphonomic damage. Additionally, Alexander (1986), following a systematic survey of brachiopod shell repair, suggested that crushing predation may have been particularly successful in those taxa (e.g. chonetids) which show little or no repair. If this is true we will never be able to distinguish between taxa which are virtually immune to predation and those which are particularly vulnerable! Other predators, such as extra-oral feeding starfish, which prise apart their valved prey, may leave no damage at all. However, predators which bore holes in the hardparts of their prey, through which they extract tissue, leave behind tangible signs which often survive taphonomic processes. Criteria for the recognition of predatory boreholes and for distinguishing them from those made by non-predatory means have been discussed by Carriker and Yochelson (1968) and Baumiller (1996). These chiefly centre on the requirement that the hole should be perpendicular to the valve surface and be generally restricted to one hole per prey item. In Recent communities the main shell boring predators are muricid and naticid gastropods, but predatory holes are also made by other gastropod taxa, octopods, and worms (see Kabat, 1990; Ponder and Taylor, 1992; Morton and Chan, 1997). Possible predatory boreholes have been recognised in a number of Palaeozoic brachiopods (e.g. Rohr, 1976; Sheehan and Lesperance, 1978;
Ausich and Gurrola, 1979; Smith et al., 1985; Chatterton and Whitehead, 1987; Conway Morris and Bengston, 1994), although some caution is required in these interpretations (Carriker and Yochelson, 1968; Harper et al., 1999). There are few reported predatory boreholes in Mesozoic brachiopods — those reported and figured by Fischer (1966) were rejected by Sohl (1969), at least as gastropod holes, on the grounds that neither muricids or naticids (the only predatory boring gastropods recognised at that time) were extant. Three putative boreholes in Jurassic rhynchonellids described and figured by Kowalewski et al. (1998) may well have been caused by a predator, but their ragged appearance suggests that they have been subject to a certain amount of taphonomic alteration which prevents clear recognition. Nevertheless, it has become clear that Mesozoic bivalves were subject to predation by boring predators (Newton, 1983; Taylor et al., 1983; Fu¨rsich and Jablonski, 1984; Newton et al., 1987; Harper et al., 1998, Kowalewski et al., 1998) and it seems reasonable to expect that such predators might also have been able to attack brachiopods. This study, therefore, concentrates on documenting boring predation on Mesozoic articulate brachiopods.
2. Materials and methods Each of the several thousand specimens of Mesozoic articulate brachiopods housed in the Sedgwick Museum (SM ) ( University of Cambridge) were individually examined and those with boreholes were retained for further inspection. Doubtful boreholes, in particular those with ragged circumferences, were rejected even though this probably resulted in the lack of recognition of some specimens in which a borehole had been masked by subsequent taphonomic damage. Very fine holes <0.3 mm (most of which were oblique to the valve surfaces) were also rejected. Where at least two holes were recorded on different valves of the same individual, care was taken to ensure that they could not be connected by a straight line, that is, that there was no possibility that they
E.M. Harper, D.S. Wharton / Palaeogeography, Palaeoclimatology, Palaeoecology 158 (2000) 15–24
17
Table 1 Evidence of boreholes in Mesozoic brachiopods recorded in this study (R, rhynchonellid prey; T, terebratulid prey) Geological age/stratigraphic horizon Cretaceous Unspecified Cretaceous
Maastrichtian Chalk Lunata Zone
Chalk Mucronata subzone Chalk, Marsupites Zone Chalk, Coranguinum Zone Chalk, Cortestudinarium Zone Turonian Chalk, planus Zone Chalk, Quadratus Zone Craie de Villedieu Cuvieri Zone Cenomanian Totternhoe Stone Cenomanian Albian/Cenomanian Warminster Greensand Red Chalk Red Chalk Albian/Aptian Lower Greensand Lower Greensand Lower Greensand Lower Greensand Lower Greensand Lower Greensand Lower Greensand Lower Greensand Lower Greensand Aptian Hythe Beds Jurassic Jurakalk Oxfordian Calcareous Grit Callovian Bathonian Great Oolite Bathonian, Great Oolite Bathonian Great Oolite Bajocian Inferior Oolite Middle Lias Middle Lias Triassic No boreholes recorded a Key localities used for statistical analyses.
Localilty
Number of bored specimens
Harvik, Sweden Luckansley, UK Le Mans, France Cambridge, UK Tournay
4R 2R 1R 3R 1T, 2R
Trimingham, Norfolk, UK Winchester, UK Warmshill, UK Norwich, Norfolk, UK Meudan, France Airesford, UK Brighton, UK Gravesend, UK Guildford, UK
14Ra 1R 1R 8R 3R 1R 1R 1R 2R
Norfolk, UK Southampton, UK Villedieu, France Wandlebury, UK Dover, UK
2R 2R 2R 2R 1R
Cambridge, UK Beer Head, UK
2R 12Ra
Warminster, UK Speeton, UK Hunstanton, UK
64Ra 1T 1T
Brickhill, Bucks., UK Campton, UK Faringdon, UK Goldaming, UK Guildford, UK Shackleford, UK Shanklin, Isle of Wight, UK Shenley Hill, Beds., UK Upware, UK Ashford, UK
15Ta 1T 1T, 2R 4T, 2R 1T 1T, 2R 3T, 1R 13Ta, 10Ra 8R 1T
Streitberg Malton, UK Montbizot, France Langton Herring, Dorset UK Bath, UK Burton Bradstock, Dorset, UK Dundry, Somerset, UK Vieux Pont, Calvados, France Yeovil, Somerset, UK
1T,1R 1T 1T 4R 1T 1T 1T 1T 1T
18
E.M. Harper, D.S. Wharton / Palaeogeography, Palaeoclimatology, Palaeoecology 158 (2000) 15–24
were produced by passage of an endolith (Richards and Shabica, 1969). For each holed valve the following data were recorded: whether the penetrated valve was brachial or pedicle, valve length (to the nearest 0.1 mm), the number of boreholes present and the hole diameter (measured to the nearest 0.01 mm). All measurements were made with vernier calipers. The position of each borehole was marked on a master diagram for each taxon. We have not sought to verify the specific and generic taxonomy of the brachiopods that we studied; instead we have contented ourselves with designating them as either rhynchonellids or terebratulids and analysed the results in these higher taxa. Inevitably this means that the groups may contain more than one species, but in practice most are dominated by a single species.
to 2.40 mm in diameter. All were apparently straight-sided, that is, they conformed to the descriptions of the ichnotaxon Oichnus simplex Bromley (1981) and none appeared to have a countersunk morphology [i.e. classified as Oichnus paraboloides Bromley (1981)]. However, as noted by some authors (e.g. Taylor et al., 1983) for bivalves, the relatively thin shells of brachiopods may make it difficult to distinguish the countersunk morphology. Meaningful understanding of predatory behaviour is only possible where a number of specimens come from a particular locality or horizon and so, following Vermeij et al. (1989), further analysis was only undertaken on taxa from single localities or horizons where there were ten or more bored individuals. This threshold is exceeded by six sets of data ( Table 2), unfortunately all of them Cretaceous: rhynchonellids from Shenley (Bedfordshire, UK ), Warminster ( Wiltshire, UK ), Southern Devon and Trimingham (Norfolk, UK ) and terebratulids from Shenley and Brickhill (Bedfordshire, UK ). The following analysis of predation patterns is, therefore, based largely on data from these key localities
3. Results and analyses Our survey revealed a total of 213 predatory boreholes in Mesozoic brachiopods (157 in rhynchonellid taxa and 56 in terebratulid taxa) from over 40 different localities ( Table 1 — the raw data, complete with museum numbers for each specimen are available on request from the authors). The majority were collected from UK localities but this reflects the predominantly British nature of the Sedgwick Museum collections rather than any particular geographic pattern. Similarly, no particular significance should be attached to the lack of Triassic boreholes, as there were very few brachiopods of this age available for study. All the recognised boreholes were circular with sharp-edges (Fig. 1) and ranged in size from 0.68
3.1. Predation frequency In direct contrast to bivalves which are usually disarticulated, it should be possible to gain a good impression of the rate of boring predation on brachiopods by calculating the percentage of articulated individuals which had been bored (although as Vermeij (1980) observed this may be an overestimate if there was a significant amount of crushing predation (e.g. by crabs) which removed unbored individuals from the record). Predation frequency
Table 2 Summary of boring predation from the five key localities (B and P refer to brachial and pedicle valves, respectively) Locality/stratigraphy
Principal prey taxa
No. of boreholes (No. B:No. P)
No. of multiply bored valves
Trimingham (Chalk:lunata zone) Devon, Cenomanian Warminster Cenomanian/Albian Shenley Hill Lower Greensand Shenley Hill Lower Greensand Brickhill Lower Greensand
Rhynchonella plicatilis Rhynchonella dimidiata Rhynchonella grassiana Rhynchonella sp. Kingena newtonii Terebratula depressa
14 12 64 10 13 15
0 0 7 1 0 0
7B:7P 8B:4P 28B:36P 5B:5P 5B:8P 9B:6P
E.M. Harper, D.S. Wharton / Palaeogeography, Palaeoclimatology, Palaeoecology 158 (2000) 15–24
19
Fig. 1. Predatory boreholes in Mesozoic brachiopods. Scale bars=10 mm. (A) Terebratula (Kingena) sp. SM B30351. Shenley Limestone, Shenley (Bedfordshire) UK; (B) Rhynchonella plicatilis J. Sowerby SM B 52653. Chalk (Lunata Zone) Trimingham (Norfolk) UK.; (C ) Terebratula (Waldheimia) numismalis Lamarck SM X29426 MiddleLiassic, Vieux Pont, Calvados, France; (D) Cretirhynchia magna Pettitt (Holotype) SM B526623. Chalk (Lunata Zone), Trimingham (Norfolk) UK.
cannot be assessed from most museum collections (see Discussion), but this was possible in one sample, from the Warminster Greensand (SM X.29402-26), obviously collected in bulk. Of 127 specimens, 58 were bored, i.e. a predation rate of some 31.4%. Despite the fact that a similar estimate could not be made for the other collections where the collection method was unknown it is clear that for each of the five other key localities boring predation was not infrequent. 3.2. Borehole positioning Boreholes were identified in both brachial and pedicle valves of the brachiopods investigated. Intuitively, given the life position of pedunculate
brachiopods, there would seem to be no good reason why one valve should be attacked more often than the other. A x2 analysis of the data failed to reject this null hypothesis (at the 5% level of significance) at any of the key localities. The borehole positioning for each of the key localities is plotted in Fig. 2 and shows a preference for boring away from the valve margins with most located either centrally or anteriorly. This preferred borehole siting was directly above the bulk of the brachiopod body mass and also coincided with the smoother parts of the valve where crenulations were not developed. Although there were individuals where boreholes occurred in a more marginal position, there were no observed instances of edge-boring, a strategy employed by
20
E.M. Harper, D.S. Wharton / Palaeogeography, Palaeoclimatology, Palaeoecology 158 (2000) 15–24
Fig. 2. Borehole positioning for each of the key localities: (A) Trimingham; (B) Devon; (C ) Shenley; (D) Warminster; ( E ) Shenley; (F ) Brickhill. For stratigraphic information see Table 1.
some gastropods on some bivalve prey ( Taylor, 1980; Vermeij, 1980). 3.3. Size relationships There is good evidence that many Recent predators, including boring gastropods, feed optimally (Hughes, 1980); predators select prey with the highest energy yield and as a result larger predators tend to take larger prey. It may be possible to identify this behaviour in the fossil record by using borehole diameter as a proxy for predator size (Carriker and Van Zandt, 1972; Wiltse, 1980 but see Harper and Morton, 1997). Borehole size was plotted against valve length for each of the six subsets of brachiopod prey ( Fig. 3) but there was no statistically significant correlation (at the 5% level ) between these parameters.
bored. Most multiply bored individuals had two holes, with a maximum of three recorded in three individuals. Prey with multiple boreholes are often assumed to have suffered a number of unsuccessful predation attempts, often signified by incomplete holes, before finally succumbing to one successful attempt. Large numbers of complete holes in an individual may be taken as evidence of prey unpalatability repelling predators once they have completely perforated the shell ( Kitchell et al., 1986; Smith et al., 1985). Unfortunately this cannot be tested in this instance because the tendency for brachiopods to be preserved in their articulated state, often with sediment or diagenetic infills, makes it difficult to confidently designate holes as complete or incomplete. Nevertheless the general impression gained from during this study was that the vast majority of holes were complete penetrations.
3.4. Multiple and incomplete boreholes 4. Discussion Relatively few brachiopods were penetrated by more than one borehole, although 12% of the Warminster Greensand brachiopods were multiply
Museum collections are clearly not the ideal place to undertake some studies in predation:
E.M. Harper, D.S. Wharton / Palaeogeography, Palaeoclimatology, Palaeoecology 158 (2000) 15–24
21
Fig. 3. Borehole diameter versus prey size for each of the key localities localities: (A) Trimingham; (B) Devon; (C ) Shenley; (D) Warminster; ( E ) Shenley; (F ) Brickhill. For stratigraphic information see Table 1.
22
E.M. Harper, D.S. Wharton / Palaeogeography, Palaeoclimatology, Palaeoecology 158 (2000) 15–24
unknown collector bias may distort, for example, the relative number of bored and unbored individuals in a sample. However, systematic surveying of large museum collections does allow the identification of whether a particular phenomenon, such as predatory boreholes, does occur at a particular geological time or in a particular geographic area and the identification of some aspects of predatory behaviour such as stereotypy. Such exercises also permit the profitable linking of small amounts of data which might otherwise be of limited use either because they are ignored (e.g. Sohl, 1969) or because they are published as anecdotal accounts. This survey has shown that Jurassic and Cretaceous terebratulid and rhynchonellid brachiopods from a wide range of localities bear relatively large, clear circular holes which fulfil the general criteria for predatory boreholes. Locally, for example in the Warminster Greensand (Albian), this type of predation may have accounted for a significant proportion of mortalities. The size of the boreholes suggests that the predators involved were relatively large and their neat circular shape suggests strongly that they were produced by chemical means (Carriker, 1981). As noted by Bromley (1981) it is not possible to identify unequivocally the perpetrators of boring predation. However, there is extremely good evidence to suggest that boring muricid and naticid gastropods, both of which are major predators in Recent communities, had evolved the boring habit by the Lower Cretaceous (Albian) ( Taylor et al., 1983) and, given the borehole morphology and the epifaunal life-habit of the prey, that most boreholes in Cretaceous brachiopods surveyed were caused by muricid gastropods. The predators responsible for the pre-Albian holes are more problematic. Fu¨rsich and Jablonski (1984), Harper et al. (1998) and Kowalewski et al. (1998) have shown that large gastropod-like boreholes are not infrequent in a range of pre-Cretaceous bivalve prey. Given the recent realization that there are at least four different clades of Recent predatory boring gastropods it is not improbable that in the past there have been other gastropods with this ability (Harper et al., 1998). Indeed Harper et al. (1999) point out that large chemically
derived boreholes occur in prey since at least the Devonian. Certainly, the ability to bore has been demonstrated for an extinct Carboniferous platyceratid gastropod by Baumiller (1990), who suggested that it was ectoparasitic rather than predatory. In many respects the identity of the predator(s) concerned is not a very important issue, although clearly it would be desirable to know. What is important is to establish that predators could attack brachiopod prey and leave some record of this activity and also to determine whether predation was frequent enough to have any real selection pressure on the prey evolution. It seems that in the Warminster Greensand at least, and probably the other key localities, brachiopods were frequently attacked by boring predators. Stereotyped borehole positioning in Recent gastropods is mostly a learned response, maintained by monotonic feeding patterns (Hughes and Dunkin, 1984; Hart and Palmer, 1987) suggesting that the predators responsible for the stereotyped feeding patterns in Mesozoic brachiopods fed on them frequently. It is highly likely that in communities with a mixed brachiopod and bivalve fauna, the bivalves, with their higher flesh yield could have been preferred prey ( Thayer, 1985; Peck, 1993). Such a supposition is difficult to test, however, as the recognition of boreholes in Mesozoic prey is strongly controlled by the taphonomy of originally aragonitic prey items (Harper et al., 1998, 1999). Nevertheless there is some support for this notion in the Blackdown Greensand fauna. Where shell preservation by silicification has allowed the recognition of frequent boring predation in a range of molluscan prey we have found no recognisable boreholes in the abundant brachiopod fauna.
5. Summary This study has shown that Mesozoic brachiopods from a range of localities were certainly attacked by boring predators. It does not support the contention that brachiopods are virtually immune to predation pressure. Rather, this research underlines the importance of this form of predation during the Mesozoic and suggests that
E.M. Harper, D.S. Wharton / Palaeogeography, Palaeoclimatology, Palaeoecology 158 (2000) 15–24
predation may have been an effective selection pressure on brachiopod taxa. There is a clear need for detailed fieldwork on boring predation levels on brachiopods from specific sites.
Acknowledgements EMH is grateful for her Royal Society University Research Fellowship and DSW worked on this project while employed at the Sedgwick Museum. The authors are grateful to Dudley Simmons for taking the photographs. This is Cambridge Earth Sciences Publication 5669.
References Alexander, R.R., 1986. Frequency of sublethal shell-breakage in articulate brachiopod assemblages through geologic time, Rachebouef, P.R., Emig, C.C. ( Eds.), Biostratigraphie du Paleozoique 4, 150–166. Ausich, W.I., Gurrola, R.A., 1979. Two boring organisms in a Lower Mississippian community of southern Indiana. J. Paleont. 53, 335–344. Baumiller, T.K., 1990. Non-predatory drilling of Mississippian crinoids by platyceratid gastropods. Palaeontology 33, 743–748. Baumiller, T.K., 1996. Boreholes in the Middle Devonian blastoid Heteroschisma and their implications for gastropod drilling. Palaeogeog. Palaeoclimatol. Palaeoecol. 123, 343–351. Bromley, R.G., 1981. Concepts in ichnotaxonomy illustrated by small round holes in shells. Acta Geol. Hisp. 16, 55–64. Carriker, M.R., 1981. Shell penetration and feeding by naticacean and muricacean predatory gastropods: a synthesis. Malacologia 20, 403–422. Carriker, M.R., Van Zandt, D., 1972. Predatory behaviour of a shell-boring muricid gastropod. In: Winn, H.E., Olla, B.L. ( Eds.), Behaviour of Marine Animals Current Perspectives in Research vol. 1. Plenum Press, New York, pp. 157–244. Carriker, M.R., Yochelson, E., 1968. Recent gastropod boreholes and Ordovician cylindrical borings. US Geol. Surv. Prof. Paper 593B, 1–26. Chatterton, B.E., Whitehead, H.L., 1987. Predatory borings in the inarticulate brachiopod Artiotreta from the Silurian of Oklahoma. Lethaia 20, 67–74. Conway Morris, S., Bengston, S., 1994. Cambrian predators: possible evidence from boreholes. J. Paleont. 68, 1–23. Curry, G.B., Ansell, A.D., 1986. Tissue mass in living brachiopods, Rachebouef, P.R., Emig, C.C. (Eds.), Biostratigraphie du Pale´ozoique 4, 231–241.
23
Donovan, S.K., Gale, A.S., 1990. Predatory asteroids and the decline of the articulate brachiopods. Lethaia 23, 77–86. Fischer, P.-H., 1966. Au sujet des perforations attribue´es des gaste´ropodes pre´-Tertiaires. J. Conchyl. 104, 45–47. Fu¨rsich, F.T., Jablonski, D., 1984. Late Triassic naticid drillholes: carnivorous gastropods gain a major adaptation but fail to radiate. Science 224, 78–80. Harper, E., Morton, B., 1997. Muricid predation upon an under-boulder community of epibyssate bivalves in the Cape d’Aguilar Marine reserve Hong Kong. In: Morton, B. ( Ed.), The Marine Flora and Fauna of Hong Kong and Southern China IV. Hong Kong University Press, Hong Kong, pp. 263–284. Harper, E.M., Forsythe, G.T.W., Palmer, T., 1998. Taphonomy and the Mesozoic Marine Revolution: preservation state masks the importance of boring predators. Palios 13, 352–360. Harper, E.M., Forsythe, G.T.W., Palmer, T., 1999. A fossil record full of holes: the Phanerozoic history of drilling predation: Reply. Geology 27, 959. Hart, M.W., Palmer, A.R., 1987. Stereotypy, ontogeny, and heritability of drill site selection in thaidid gastropods. J. Exp. Mar. Biol. Ecol. 107, 101–120. Hughes, R.N., 1980. Optimal foraging theory in the marine context. Oceanogr. Mar. Biol. Ann. Rev. 18, 423–481. Hughes, R.N., Dunkin, S., 1984. Behavioural components of prey selection by dogwhelks, Nucella lapillus (L.) feeding on mussels in the laboratory. J. Exp. Mar. Biol. Ecol. 77, 45–68. Kabat, A.R., 1990. Predatory ecology of naticid gastropods with a review of shell boring. Malacologia 32, 155–193. Kitchell, J.A., Boggs, C.H., Rice, J.A., Kitchell, J.F., Hoffman, A., Martinell, A., 1986. Anomalies in naticid predatory behavior: a critique and experimental observations. Malacologia 27, 291–298. Kowalewski, M., Dulai, A., Fu¨rsich, F.T., 1998. A fossil record full of holes: the Phanerozoic history of drilling predation. Geology 26, 1091–1094. Mauzey, K.P., Birkeland, C., Dayton, P.K., 1968. Feeding behaviour of asteroids and escape responses of prey in the Puget Sound region. Ecology 49, 603–619. Morton, B., Chan, K., 1997. First report of shell boring predation by a member of the Nassariidae (Gastropoda). J. Moll. Stud. 63, 476–478. Newton, C.R., 1983. Triassic origin of shell-boring gastropods. Geol Soc. Am. Abstr. Progr. 15, 652–653. Newton, C.R., Whalen, M.T., Thompson, J.B., Prins, N., Dellala, D., 1987. Systematics and paleoecology of Norian (Late Triassic) bivalves from a tropical island arc: Wallowa Terrane Oregon. Paleont. Soc Mem., J. Paleont. 61, 1–83. Noble, J.P.A., Logan, A., 1981. Size frequency distributions and taphonomy of brachiopods: a recent model. Palaeogeog. Palaeoclimatol. Palaeoecol. 36, 87–105. Peck, L.S., 1993. The tissues of articulate brachiopods and their value to predators. Phil. Trans. R. Soc., Lond. B 339, 17–32. Ponder, W.F., Taylor, J.D., 1992. Predatory shell drilling by two species of Austroginella (Gastropoda: Marginellidae). J. Zool. Lond. 228, 317–328.
24
E.M. Harper, D.S. Wharton / Palaeogeography, Palaeoclimatology, Palaeoecology 158 (2000) 15–24
Richards, R.P., Shabica, C.W., 1969. Cylindrical living burrows in Ordovician dalmanellid brachiopod beds. J. Paleont. 43, 838–841. Rohr, D.M., 1976. Silurian predator borings in the brachiopod Dicaelosia from the Canadian Arctic. J. Paleont. 50, 1175–1179. Rudwick, M.J., 1970. Living and Fossil Brachiopods. Hutchinson University Library, London. Sheehan, P.M., Lesperance, P.J., 1978. Effect of predation on the population dynamics of a Devonian brachiopod. J. Paleont. 52, 812–817. Smith, S.A., Thayer, C.W., Brett, C.E., 1985. Predation in the Paleozoic: gastropod-like drillholes in Devonian brachiopods. Science 230, 1033–1035. Sohl, N.F., 1969. The fossil record of shell boring by snails. Am. Zool. 9, 725–734. Stanley, S.M., 1974. What has happened to the articulate brachiopods. Geol Soc. Am. Abstr. Progr. 6, 966–967. Stanley, S.M., 1977. Trends rates and patterns of evolution in the Bivalvia. In: Hallam, A. (Ed.), Patterns of Evolution as Illustrated by the Fossil Record. Elsevier, Amsterdam, pp. 209–250. Stanley, S.M., 1979. Macroevolution: Pattern and Process. Freeman, San Francisco. Taylor, J.D., 1980. Diets and habitats of shallow water predatory gastropods around Tolo Channel Hong Kong. In: Morton, B. ( Ed.), The Malacofauna of Hong Kong: The Proceedings of the First International Workshop on the Malacofauna of Hong Kong and Southern China, 1977. Hong Kong University Press, Hong Kong, pp. 163–180.
Taylor, J.D., Cleevely, R.J., Morris, N.J., 1983. Predatory gastropods and their activities in the Blackdown Greensand (Albian) of England. Palaeontology 26, 521–533. Thayer, C.W., 1981. Ecology of living brachiopods. In: Broadhead, T.W. ( Ed.), Lophophorates: Notes for a Short Course No. 5. University of Tennessee, Department of Geology, Cincinnati, pp. 110–126. Thayer, C.W., 1985. Brachiopods versus mussels: competition, predation and palatability. Science 228, 1527–1528. Thayer, C.W., Allmon, R., 1990. Unpalatable thecideid brachiopods from Palau: ecological and evolutionary implications. In: MacKinnon, L., Campbell, A. ( Eds.), Brachiopods through Time. Balkema, Rotterdam, pp. 253–260. Vermeij, G.J., 1980. Drilling predation of bivalves in Guam: some paleoecological implications. Malacologia 19, 329–334. Vermeij, G.J., 1983. Traces and trends in predation, with special reference to bivalved animals. Palaeontology 26, 455–465. Vermeij, G.J., Dudley, E.C., Zipser, E., 1989. Successful and unsuccessful drilling predation in Recent pelecypods. Veliger 32, 266–273. Wiltse, L.W., 1980. Predation by juvenile Polinices duplicatus (Say) on Gemma ( Totten). J. Exp. Mar. Biol. Ecol. 42, 187–199. Witman, J.D., Cooper, R.A., 1983. Disturbance and contrasting patterns of population structure in the brachiopod Terebratulina septentrionalis (Couthouy) from two subtidal habitats). J. Exp. Mar. Biol. Ecol. 73, 57–79.
Boring predation and Mesozoic articulate brachiopods E.M. Harper *, D.S. Wharton 1 Department of Earth Sciences, Downing Street, Cambridge CB2 3EQ, UK Received 8 June 1999; accepted for publication 28 October 1999
Abstract A systematic survey of all the Mesozoic brachiopods in the large collections of the Sedgwick Museum (Cambridge University) has revealed more than 213 predatory boreholes from a wide range of largely British localities. It seems likely that this type of predation was not infrequent, at least locally, as evidenced by the proportion of bored valves at some localities and the degree of stereotypy shown in borehole positioning. The size of the boreholes and their neat circular cross sections suggest that they were made by large, epifaunal predators using chemical attack and those of post-Albian age may be comfortably (if not confidentally) assigned to muricid gastropods. Although it is likely that bivalves, with their greater flesh yields, were the preferred prey item in most Mesozoic shelly benthic communities, it is apparent that boring predators may have resulted in a significant predation pressure on articulate brachiopods. © 2000 Elsevier Science B.V. All rights reserved. Keywords: brachiopods; gastropods; Mesozoic; predation
1. Introduction There is a strange contradiction in the perceived importance of predation pressure on the evolution of brachiopods. On the one hand, there is a popular notion that brachiopods, articulates in particular, are unattractive to predators and have been so in the geological past (Rudwick, 1970; Thayer, 1981, 1985; Thayer and Allmon, 1990), in which case predation cannot have been an important evolutionary selection pressure. On the other hand, however, direct predation pressure on vulnerable brachiopod taxa has been used to explain why brachiopods failed to significantly re-radiate after the Permian–Triassic mass extinction (e.g. Stanley, 1974, 1977, 1979; Donovan and Gale, * Corresponding author. Fax: +44-1223-333450. E-mail address: [email protected] ( E.M. Harper) 1 Current address: Department of Geology, University of Bristol, Queen’s Road, Bristol BS8 1JR, UK.
1990), whilst Vermeij (1983) has pointed to the potential vulnerability of the bi-valved form. The supposition that brachiopods are not (and have not been) important prey items is based on two major lines of evidence. Firstly, there are few published accounts of predation on modern brachiopods and secondly, the experimental observation by Thayer (1985) that a range of modern predators appeared to prefer bivalve mussels to brachiopods. Several suggestions have advanced for this apparent lack of predation pressure: 1. their low body mass, up to 50% of which is not readily accessible in punctate taxa (Curry and Ansell, 1986) which makes them unattractive in comparison to bivalves with their greater yield; and 2. a lack of palatability due to spicules within the flesh and the possibility that their tissues may contain toxins ( Thayer, 1985; Thayer and Allmon, 1990).
0031-0182/00/$ - see front matter © 2000 Elsevier Science B.V. All rights reserved. PII: S0 0 3 1 -0 1 8 2 ( 9 9 ) 0 0 16 4 - 9
16
E.M. Harper, D.S. Wharton / Palaeogeography, Palaeoclimatology, Palaeoecology 158 (2000) 15–24
It should be noted, however, that to date no toxins have been isolated from brachiopod tissue (Peck, 1993). Nevertheless, there are records of predation on Recent articulate brachiopods by a range of modern predators, for example, fish ( Witman and Cooper, 1983), asteroids (Mauzey et al., 1968) and gastropods (Noble and Logan, 1981; Witman and Cooper, 1983). It is difficult to believe that ancient brachiopods did not suffer similar predation, particularly during the Palaeozoic and Mesozoic when they formed an important part of the shelly benthos. However, reports of predated fossil articulates are relatively few and most are based on Palaeozoic material. The victims of many predatory methods may not always be readily identified in the fossil record; for example it is difficult to distinguish damage inflicted by crushing predators from taphonomic damage. Additionally, Alexander (1986), following a systematic survey of brachiopod shell repair, suggested that crushing predation may have been particularly successful in those taxa (e.g. chonetids) which show little or no repair. If this is true we will never be able to distinguish between taxa which are virtually immune to predation and those which are particularly vulnerable! Other predators, such as extra-oral feeding starfish, which prise apart their valved prey, may leave no damage at all. However, predators which bore holes in the hardparts of their prey, through which they extract tissue, leave behind tangible signs which often survive taphonomic processes. Criteria for the recognition of predatory boreholes and for distinguishing them from those made by non-predatory means have been discussed by Carriker and Yochelson (1968) and Baumiller (1996). These chiefly centre on the requirement that the hole should be perpendicular to the valve surface and be generally restricted to one hole per prey item. In Recent communities the main shell boring predators are muricid and naticid gastropods, but predatory holes are also made by other gastropod taxa, octopods, and worms (see Kabat, 1990; Ponder and Taylor, 1992; Morton and Chan, 1997). Possible predatory boreholes have been recognised in a number of Palaeozoic brachiopods (e.g. Rohr, 1976; Sheehan and Lesperance, 1978;
Ausich and Gurrola, 1979; Smith et al., 1985; Chatterton and Whitehead, 1987; Conway Morris and Bengston, 1994), although some caution is required in these interpretations (Carriker and Yochelson, 1968; Harper et al., 1999). There are few reported predatory boreholes in Mesozoic brachiopods — those reported and figured by Fischer (1966) were rejected by Sohl (1969), at least as gastropod holes, on the grounds that neither muricids or naticids (the only predatory boring gastropods recognised at that time) were extant. Three putative boreholes in Jurassic rhynchonellids described and figured by Kowalewski et al. (1998) may well have been caused by a predator, but their ragged appearance suggests that they have been subject to a certain amount of taphonomic alteration which prevents clear recognition. Nevertheless, it has become clear that Mesozoic bivalves were subject to predation by boring predators (Newton, 1983; Taylor et al., 1983; Fu¨rsich and Jablonski, 1984; Newton et al., 1987; Harper et al., 1998, Kowalewski et al., 1998) and it seems reasonable to expect that such predators might also have been able to attack brachiopods. This study, therefore, concentrates on documenting boring predation on Mesozoic articulate brachiopods.
2. Materials and methods Each of the several thousand specimens of Mesozoic articulate brachiopods housed in the Sedgwick Museum (SM ) ( University of Cambridge) were individually examined and those with boreholes were retained for further inspection. Doubtful boreholes, in particular those with ragged circumferences, were rejected even though this probably resulted in the lack of recognition of some specimens in which a borehole had been masked by subsequent taphonomic damage. Very fine holes <0.3 mm (most of which were oblique to the valve surfaces) were also rejected. Where at least two holes were recorded on different valves of the same individual, care was taken to ensure that they could not be connected by a straight line, that is, that there was no possibility that they
E.M. Harper, D.S. Wharton / Palaeogeography, Palaeoclimatology, Palaeoecology 158 (2000) 15–24
17
Table 1 Evidence of boreholes in Mesozoic brachiopods recorded in this study (R, rhynchonellid prey; T, terebratulid prey) Geological age/stratigraphic horizon Cretaceous Unspecified Cretaceous
Maastrichtian Chalk Lunata Zone
Chalk Mucronata subzone Chalk, Marsupites Zone Chalk, Coranguinum Zone Chalk, Cortestudinarium Zone Turonian Chalk, planus Zone Chalk, Quadratus Zone Craie de Villedieu Cuvieri Zone Cenomanian Totternhoe Stone Cenomanian Albian/Cenomanian Warminster Greensand Red Chalk Red Chalk Albian/Aptian Lower Greensand Lower Greensand Lower Greensand Lower Greensand Lower Greensand Lower Greensand Lower Greensand Lower Greensand Lower Greensand Aptian Hythe Beds Jurassic Jurakalk Oxfordian Calcareous Grit Callovian Bathonian Great Oolite Bathonian, Great Oolite Bathonian Great Oolite Bajocian Inferior Oolite Middle Lias Middle Lias Triassic No boreholes recorded a Key localities used for statistical analyses.
Localilty
Number of bored specimens
Harvik, Sweden Luckansley, UK Le Mans, France Cambridge, UK Tournay
4R 2R 1R 3R 1T, 2R
Trimingham, Norfolk, UK Winchester, UK Warmshill, UK Norwich, Norfolk, UK Meudan, France Airesford, UK Brighton, UK Gravesend, UK Guildford, UK
14Ra 1R 1R 8R 3R 1R 1R 1R 2R
Norfolk, UK Southampton, UK Villedieu, France Wandlebury, UK Dover, UK
2R 2R 2R 2R 1R
Cambridge, UK Beer Head, UK
2R 12Ra
Warminster, UK Speeton, UK Hunstanton, UK
64Ra 1T 1T
Brickhill, Bucks., UK Campton, UK Faringdon, UK Goldaming, UK Guildford, UK Shackleford, UK Shanklin, Isle of Wight, UK Shenley Hill, Beds., UK Upware, UK Ashford, UK
15Ta 1T 1T, 2R 4T, 2R 1T 1T, 2R 3T, 1R 13Ta, 10Ra 8R 1T
Streitberg Malton, UK Montbizot, France Langton Herring, Dorset UK Bath, UK Burton Bradstock, Dorset, UK Dundry, Somerset, UK Vieux Pont, Calvados, France Yeovil, Somerset, UK
1T,1R 1T 1T 4R 1T 1T 1T 1T 1T
18
E.M. Harper, D.S. Wharton / Palaeogeography, Palaeoclimatology, Palaeoecology 158 (2000) 15–24
were produced by passage of an endolith (Richards and Shabica, 1969). For each holed valve the following data were recorded: whether the penetrated valve was brachial or pedicle, valve length (to the nearest 0.1 mm), the number of boreholes present and the hole diameter (measured to the nearest 0.01 mm). All measurements were made with vernier calipers. The position of each borehole was marked on a master diagram for each taxon. We have not sought to verify the specific and generic taxonomy of the brachiopods that we studied; instead we have contented ourselves with designating them as either rhynchonellids or terebratulids and analysed the results in these higher taxa. Inevitably this means that the groups may contain more than one species, but in practice most are dominated by a single species.
to 2.40 mm in diameter. All were apparently straight-sided, that is, they conformed to the descriptions of the ichnotaxon Oichnus simplex Bromley (1981) and none appeared to have a countersunk morphology [i.e. classified as Oichnus paraboloides Bromley (1981)]. However, as noted by some authors (e.g. Taylor et al., 1983) for bivalves, the relatively thin shells of brachiopods may make it difficult to distinguish the countersunk morphology. Meaningful understanding of predatory behaviour is only possible where a number of specimens come from a particular locality or horizon and so, following Vermeij et al. (1989), further analysis was only undertaken on taxa from single localities or horizons where there were ten or more bored individuals. This threshold is exceeded by six sets of data ( Table 2), unfortunately all of them Cretaceous: rhynchonellids from Shenley (Bedfordshire, UK ), Warminster ( Wiltshire, UK ), Southern Devon and Trimingham (Norfolk, UK ) and terebratulids from Shenley and Brickhill (Bedfordshire, UK ). The following analysis of predation patterns is, therefore, based largely on data from these key localities
3. Results and analyses Our survey revealed a total of 213 predatory boreholes in Mesozoic brachiopods (157 in rhynchonellid taxa and 56 in terebratulid taxa) from over 40 different localities ( Table 1 — the raw data, complete with museum numbers for each specimen are available on request from the authors). The majority were collected from UK localities but this reflects the predominantly British nature of the Sedgwick Museum collections rather than any particular geographic pattern. Similarly, no particular significance should be attached to the lack of Triassic boreholes, as there were very few brachiopods of this age available for study. All the recognised boreholes were circular with sharp-edges (Fig. 1) and ranged in size from 0.68
3.1. Predation frequency In direct contrast to bivalves which are usually disarticulated, it should be possible to gain a good impression of the rate of boring predation on brachiopods by calculating the percentage of articulated individuals which had been bored (although as Vermeij (1980) observed this may be an overestimate if there was a significant amount of crushing predation (e.g. by crabs) which removed unbored individuals from the record). Predation frequency
Table 2 Summary of boring predation from the five key localities (B and P refer to brachial and pedicle valves, respectively) Locality/stratigraphy
Principal prey taxa
No. of boreholes (No. B:No. P)
No. of multiply bored valves
Trimingham (Chalk:lunata zone) Devon, Cenomanian Warminster Cenomanian/Albian Shenley Hill Lower Greensand Shenley Hill Lower Greensand Brickhill Lower Greensand
Rhynchonella plicatilis Rhynchonella dimidiata Rhynchonella grassiana Rhynchonella sp. Kingena newtonii Terebratula depressa
14 12 64 10 13 15
0 0 7 1 0 0
7B:7P 8B:4P 28B:36P 5B:5P 5B:8P 9B:6P
E.M. Harper, D.S. Wharton / Palaeogeography, Palaeoclimatology, Palaeoecology 158 (2000) 15–24
19
Fig. 1. Predatory boreholes in Mesozoic brachiopods. Scale bars=10 mm. (A) Terebratula (Kingena) sp. SM B30351. Shenley Limestone, Shenley (Bedfordshire) UK; (B) Rhynchonella plicatilis J. Sowerby SM B 52653. Chalk (Lunata Zone) Trimingham (Norfolk) UK.; (C ) Terebratula (Waldheimia) numismalis Lamarck SM X29426 MiddleLiassic, Vieux Pont, Calvados, France; (D) Cretirhynchia magna Pettitt (Holotype) SM B526623. Chalk (Lunata Zone), Trimingham (Norfolk) UK.
cannot be assessed from most museum collections (see Discussion), but this was possible in one sample, from the Warminster Greensand (SM X.29402-26), obviously collected in bulk. Of 127 specimens, 58 were bored, i.e. a predation rate of some 31.4%. Despite the fact that a similar estimate could not be made for the other collections where the collection method was unknown it is clear that for each of the five other key localities boring predation was not infrequent. 3.2. Borehole positioning Boreholes were identified in both brachial and pedicle valves of the brachiopods investigated. Intuitively, given the life position of pedunculate
brachiopods, there would seem to be no good reason why one valve should be attacked more often than the other. A x2 analysis of the data failed to reject this null hypothesis (at the 5% level of significance) at any of the key localities. The borehole positioning for each of the key localities is plotted in Fig. 2 and shows a preference for boring away from the valve margins with most located either centrally or anteriorly. This preferred borehole siting was directly above the bulk of the brachiopod body mass and also coincided with the smoother parts of the valve where crenulations were not developed. Although there were individuals where boreholes occurred in a more marginal position, there were no observed instances of edge-boring, a strategy employed by
20
E.M. Harper, D.S. Wharton / Palaeogeography, Palaeoclimatology, Palaeoecology 158 (2000) 15–24
Fig. 2. Borehole positioning for each of the key localities: (A) Trimingham; (B) Devon; (C ) Shenley; (D) Warminster; ( E ) Shenley; (F ) Brickhill. For stratigraphic information see Table 1.
some gastropods on some bivalve prey ( Taylor, 1980; Vermeij, 1980). 3.3. Size relationships There is good evidence that many Recent predators, including boring gastropods, feed optimally (Hughes, 1980); predators select prey with the highest energy yield and as a result larger predators tend to take larger prey. It may be possible to identify this behaviour in the fossil record by using borehole diameter as a proxy for predator size (Carriker and Van Zandt, 1972; Wiltse, 1980 but see Harper and Morton, 1997). Borehole size was plotted against valve length for each of the six subsets of brachiopod prey ( Fig. 3) but there was no statistically significant correlation (at the 5% level ) between these parameters.
bored. Most multiply bored individuals had two holes, with a maximum of three recorded in three individuals. Prey with multiple boreholes are often assumed to have suffered a number of unsuccessful predation attempts, often signified by incomplete holes, before finally succumbing to one successful attempt. Large numbers of complete holes in an individual may be taken as evidence of prey unpalatability repelling predators once they have completely perforated the shell ( Kitchell et al., 1986; Smith et al., 1985). Unfortunately this cannot be tested in this instance because the tendency for brachiopods to be preserved in their articulated state, often with sediment or diagenetic infills, makes it difficult to confidently designate holes as complete or incomplete. Nevertheless the general impression gained from during this study was that the vast majority of holes were complete penetrations.
3.4. Multiple and incomplete boreholes 4. Discussion Relatively few brachiopods were penetrated by more than one borehole, although 12% of the Warminster Greensand brachiopods were multiply
Museum collections are clearly not the ideal place to undertake some studies in predation:
E.M. Harper, D.S. Wharton / Palaeogeography, Palaeoclimatology, Palaeoecology 158 (2000) 15–24
21
Fig. 3. Borehole diameter versus prey size for each of the key localities localities: (A) Trimingham; (B) Devon; (C ) Shenley; (D) Warminster; ( E ) Shenley; (F ) Brickhill. For stratigraphic information see Table 1.
22
E.M. Harper, D.S. Wharton / Palaeogeography, Palaeoclimatology, Palaeoecology 158 (2000) 15–24
unknown collector bias may distort, for example, the relative number of bored and unbored individuals in a sample. However, systematic surveying of large museum collections does allow the identification of whether a particular phenomenon, such as predatory boreholes, does occur at a particular geological time or in a particular geographic area and the identification of some aspects of predatory behaviour such as stereotypy. Such exercises also permit the profitable linking of small amounts of data which might otherwise be of limited use either because they are ignored (e.g. Sohl, 1969) or because they are published as anecdotal accounts. This survey has shown that Jurassic and Cretaceous terebratulid and rhynchonellid brachiopods from a wide range of localities bear relatively large, clear circular holes which fulfil the general criteria for predatory boreholes. Locally, for example in the Warminster Greensand (Albian), this type of predation may have accounted for a significant proportion of mortalities. The size of the boreholes suggests that the predators involved were relatively large and their neat circular shape suggests strongly that they were produced by chemical means (Carriker, 1981). As noted by Bromley (1981) it is not possible to identify unequivocally the perpetrators of boring predation. However, there is extremely good evidence to suggest that boring muricid and naticid gastropods, both of which are major predators in Recent communities, had evolved the boring habit by the Lower Cretaceous (Albian) ( Taylor et al., 1983) and, given the borehole morphology and the epifaunal life-habit of the prey, that most boreholes in Cretaceous brachiopods surveyed were caused by muricid gastropods. The predators responsible for the pre-Albian holes are more problematic. Fu¨rsich and Jablonski (1984), Harper et al. (1998) and Kowalewski et al. (1998) have shown that large gastropod-like boreholes are not infrequent in a range of pre-Cretaceous bivalve prey. Given the recent realization that there are at least four different clades of Recent predatory boring gastropods it is not improbable that in the past there have been other gastropods with this ability (Harper et al., 1998). Indeed Harper et al. (1999) point out that large chemically
derived boreholes occur in prey since at least the Devonian. Certainly, the ability to bore has been demonstrated for an extinct Carboniferous platyceratid gastropod by Baumiller (1990), who suggested that it was ectoparasitic rather than predatory. In many respects the identity of the predator(s) concerned is not a very important issue, although clearly it would be desirable to know. What is important is to establish that predators could attack brachiopod prey and leave some record of this activity and also to determine whether predation was frequent enough to have any real selection pressure on the prey evolution. It seems that in the Warminster Greensand at least, and probably the other key localities, brachiopods were frequently attacked by boring predators. Stereotyped borehole positioning in Recent gastropods is mostly a learned response, maintained by monotonic feeding patterns (Hughes and Dunkin, 1984; Hart and Palmer, 1987) suggesting that the predators responsible for the stereotyped feeding patterns in Mesozoic brachiopods fed on them frequently. It is highly likely that in communities with a mixed brachiopod and bivalve fauna, the bivalves, with their higher flesh yield could have been preferred prey ( Thayer, 1985; Peck, 1993). Such a supposition is difficult to test, however, as the recognition of boreholes in Mesozoic prey is strongly controlled by the taphonomy of originally aragonitic prey items (Harper et al., 1998, 1999). Nevertheless there is some support for this notion in the Blackdown Greensand fauna. Where shell preservation by silicification has allowed the recognition of frequent boring predation in a range of molluscan prey we have found no recognisable boreholes in the abundant brachiopod fauna.
5. Summary This study has shown that Mesozoic brachiopods from a range of localities were certainly attacked by boring predators. It does not support the contention that brachiopods are virtually immune to predation pressure. Rather, this research underlines the importance of this form of predation during the Mesozoic and suggests that
E.M. Harper, D.S. Wharton / Palaeogeography, Palaeoclimatology, Palaeoecology 158 (2000) 15–24
predation may have been an effective selection pressure on brachiopod taxa. There is a clear need for detailed fieldwork on boring predation levels on brachiopods from specific sites.
Acknowledgements EMH is grateful for her Royal Society University Research Fellowship and DSW worked on this project while employed at the Sedgwick Museum. The authors are grateful to Dudley Simmons for taking the photographs. This is Cambridge Earth Sciences Publication 5669.
References Alexander, R.R., 1986. Frequency of sublethal shell-breakage in articulate brachiopod assemblages through geologic time, Rachebouef, P.R., Emig, C.C. ( Eds.), Biostratigraphie du Paleozoique 4, 150–166. Ausich, W.I., Gurrola, R.A., 1979. Two boring organisms in a Lower Mississippian community of southern Indiana. J. Paleont. 53, 335–344. Baumiller, T.K., 1990. Non-predatory drilling of Mississippian crinoids by platyceratid gastropods. Palaeontology 33, 743–748. Baumiller, T.K., 1996. Boreholes in the Middle Devonian blastoid Heteroschisma and their implications for gastropod drilling. Palaeogeog. Palaeoclimatol. Palaeoecol. 123, 343–351. Bromley, R.G., 1981. Concepts in ichnotaxonomy illustrated by small round holes in shells. Acta Geol. Hisp. 16, 55–64. Carriker, M.R., 1981. Shell penetration and feeding by naticacean and muricacean predatory gastropods: a synthesis. Malacologia 20, 403–422. Carriker, M.R., Van Zandt, D., 1972. Predatory behaviour of a shell-boring muricid gastropod. In: Winn, H.E., Olla, B.L. ( Eds.), Behaviour of Marine Animals Current Perspectives in Research vol. 1. Plenum Press, New York, pp. 157–244. Carriker, M.R., Yochelson, E., 1968. Recent gastropod boreholes and Ordovician cylindrical borings. US Geol. Surv. Prof. Paper 593B, 1–26. Chatterton, B.E., Whitehead, H.L., 1987. Predatory borings in the inarticulate brachiopod Artiotreta from the Silurian of Oklahoma. Lethaia 20, 67–74. Conway Morris, S., Bengston, S., 1994. Cambrian predators: possible evidence from boreholes. J. Paleont. 68, 1–23. Curry, G.B., Ansell, A.D., 1986. Tissue mass in living brachiopods, Rachebouef, P.R., Emig, C.C. (Eds.), Biostratigraphie du Pale´ozoique 4, 231–241.
23
Donovan, S.K., Gale, A.S., 1990. Predatory asteroids and the decline of the articulate brachiopods. Lethaia 23, 77–86. Fischer, P.-H., 1966. Au sujet des perforations attribue´es des gaste´ropodes pre´-Tertiaires. J. Conchyl. 104, 45–47. Fu¨rsich, F.T., Jablonski, D., 1984. Late Triassic naticid drillholes: carnivorous gastropods gain a major adaptation but fail to radiate. Science 224, 78–80. Harper, E., Morton, B., 1997. Muricid predation upon an under-boulder community of epibyssate bivalves in the Cape d’Aguilar Marine reserve Hong Kong. In: Morton, B. ( Ed.), The Marine Flora and Fauna of Hong Kong and Southern China IV. Hong Kong University Press, Hong Kong, pp. 263–284. Harper, E.M., Forsythe, G.T.W., Palmer, T., 1998. Taphonomy and the Mesozoic Marine Revolution: preservation state masks the importance of boring predators. Palios 13, 352–360. Harper, E.M., Forsythe, G.T.W., Palmer, T., 1999. A fossil record full of holes: the Phanerozoic history of drilling predation: Reply. Geology 27, 959. Hart, M.W., Palmer, A.R., 1987. Stereotypy, ontogeny, and heritability of drill site selection in thaidid gastropods. J. Exp. Mar. Biol. Ecol. 107, 101–120. Hughes, R.N., 1980. Optimal foraging theory in the marine context. Oceanogr. Mar. Biol. Ann. Rev. 18, 423–481. Hughes, R.N., Dunkin, S., 1984. Behavioural components of prey selection by dogwhelks, Nucella lapillus (L.) feeding on mussels in the laboratory. J. Exp. Mar. Biol. Ecol. 77, 45–68. Kabat, A.R., 1990. Predatory ecology of naticid gastropods with a review of shell boring. Malacologia 32, 155–193. Kitchell, J.A., Boggs, C.H., Rice, J.A., Kitchell, J.F., Hoffman, A., Martinell, A., 1986. Anomalies in naticid predatory behavior: a critique and experimental observations. Malacologia 27, 291–298. Kowalewski, M., Dulai, A., Fu¨rsich, F.T., 1998. A fossil record full of holes: the Phanerozoic history of drilling predation. Geology 26, 1091–1094. Mauzey, K.P., Birkeland, C., Dayton, P.K., 1968. Feeding behaviour of asteroids and escape responses of prey in the Puget Sound region. Ecology 49, 603–619. Morton, B., Chan, K., 1997. First report of shell boring predation by a member of the Nassariidae (Gastropoda). J. Moll. Stud. 63, 476–478. Newton, C.R., 1983. Triassic origin of shell-boring gastropods. Geol Soc. Am. Abstr. Progr. 15, 652–653. Newton, C.R., Whalen, M.T., Thompson, J.B., Prins, N., Dellala, D., 1987. Systematics and paleoecology of Norian (Late Triassic) bivalves from a tropical island arc: Wallowa Terrane Oregon. Paleont. Soc Mem., J. Paleont. 61, 1–83. Noble, J.P.A., Logan, A., 1981. Size frequency distributions and taphonomy of brachiopods: a recent model. Palaeogeog. Palaeoclimatol. Palaeoecol. 36, 87–105. Peck, L.S., 1993. The tissues of articulate brachiopods and their value to predators. Phil. Trans. R. Soc., Lond. B 339, 17–32. Ponder, W.F., Taylor, J.D., 1992. Predatory shell drilling by two species of Austroginella (Gastropoda: Marginellidae). J. Zool. Lond. 228, 317–328.
24
E.M. Harper, D.S. Wharton / Palaeogeography, Palaeoclimatology, Palaeoecology 158 (2000) 15–24
Richards, R.P., Shabica, C.W., 1969. Cylindrical living burrows in Ordovician dalmanellid brachiopod beds. J. Paleont. 43, 838–841. Rohr, D.M., 1976. Silurian predator borings in the brachiopod Dicaelosia from the Canadian Arctic. J. Paleont. 50, 1175–1179. Rudwick, M.J., 1970. Living and Fossil Brachiopods. Hutchinson University Library, London. Sheehan, P.M., Lesperance, P.J., 1978. Effect of predation on the population dynamics of a Devonian brachiopod. J. Paleont. 52, 812–817. Smith, S.A., Thayer, C.W., Brett, C.E., 1985. Predation in the Paleozoic: gastropod-like drillholes in Devonian brachiopods. Science 230, 1033–1035. Sohl, N.F., 1969. The fossil record of shell boring by snails. Am. Zool. 9, 725–734. Stanley, S.M., 1974. What has happened to the articulate brachiopods. Geol Soc. Am. Abstr. Progr. 6, 966–967. Stanley, S.M., 1977. Trends rates and patterns of evolution in the Bivalvia. In: Hallam, A. (Ed.), Patterns of Evolution as Illustrated by the Fossil Record. Elsevier, Amsterdam, pp. 209–250. Stanley, S.M., 1979. Macroevolution: Pattern and Process. Freeman, San Francisco. Taylor, J.D., 1980. Diets and habitats of shallow water predatory gastropods around Tolo Channel Hong Kong. In: Morton, B. ( Ed.), The Malacofauna of Hong Kong: The Proceedings of the First International Workshop on the Malacofauna of Hong Kong and Southern China, 1977. Hong Kong University Press, Hong Kong, pp. 163–180.
Taylor, J.D., Cleevely, R.J., Morris, N.J., 1983. Predatory gastropods and their activities in the Blackdown Greensand (Albian) of England. Palaeontology 26, 521–533. Thayer, C.W., 1981. Ecology of living brachiopods. In: Broadhead, T.W. ( Ed.), Lophophorates: Notes for a Short Course No. 5. University of Tennessee, Department of Geology, Cincinnati, pp. 110–126. Thayer, C.W., 1985. Brachiopods versus mussels: competition, predation and palatability. Science 228, 1527–1528. Thayer, C.W., Allmon, R., 1990. Unpalatable thecideid brachiopods from Palau: ecological and evolutionary implications. In: MacKinnon, L., Campbell, A. ( Eds.), Brachiopods through Time. Balkema, Rotterdam, pp. 253–260. Vermeij, G.J., 1980. Drilling predation of bivalves in Guam: some paleoecological implications. Malacologia 19, 329–334. Vermeij, G.J., 1983. Traces and trends in predation, with special reference to bivalved animals. Palaeontology 26, 455–465. Vermeij, G.J., Dudley, E.C., Zipser, E., 1989. Successful and unsuccessful drilling predation in Recent pelecypods. Veliger 32, 266–273. Wiltse, L.W., 1980. Predation by juvenile Polinices duplicatus (Say) on Gemma ( Totten). J. Exp. Mar. Biol. Ecol. 42, 187–199. Witman, J.D., Cooper, R.A., 1983. Disturbance and contrasting patterns of population structure in the brachiopod Terebratulina septentrionalis (Couthouy) from two subtidal habitats). J. Exp. Mar. Biol. Ecol. 73, 57–79.