Environmental impact on ectocochleate cephalopod reproductive strategies and the evolutionary significance of cephalopod egg size

Abstract

Published data on initial chamber (protoconch) diameter in 507 species, and embryonic shell (ammonitella) diameter in 231 species of Ammonoidea, and embryonic shell (nauta) diameters for 132 species of coiled Nautiloidea, were used to examine evolutionary change in ectocochleate cephalopod reproductive strategies. Palaeotemperatures were found to be a key factor influencing historical changes in the evolution of egg size in ammonoids and nautiloids. A negative relationship was found between egg size and warming of the Earth's climate. Factors related to habitat were also important; in general egg size was larger in cold-water cephalopods. Egg size in Lytoceratina and Phylloceratina in the deep waters of the upper continental slope was much larger than in epipelagic Scaphitidae, as in modern fish and squids. Small eggs and high evolutionary rates helped ammonoids to colonise new habitats and develop high biological diversity, but involved them in planktonic food webs making them more vulnerable to abiotic variability (e.g., climatic changes), ultimately leading to their extinction. Large eggs helped nautiloids to persist through geological history, but at the cost of lower biological diversity, lower evolutionary rates and restricted options for colonising new habitats. Large-egged species such as nautiloids are more vulnerable to ecological, biotic disasters such as the appearance of new predators, including modern fishery. Independence from the planktonic food web is likely to be very important for a taxon's long-term survival over evolutionary history, as demonstrated also by Coelacanthiformes and Elasmobranchia. • Key words: Ammonoidea, Nautiloidea, reproductive strategy, mass extinction, climate change, egg. Vladimir V. Laptikhovsky, Falkland Islands Government Fisheries Department, Stanley, FIQQ 1ZZ, Falkland Islands; vlaptikhovsky@fisheries.gov.fk • Mikhail A. Rogov, Geological Institute of Russian Academy of Sciences, Pyzhevskii Lane 7, Moscow, 119017, Russia; russianjurassic@gmail.com • Svetlana V. Nikolaeva, Paleontological Institute, Russian Academy of Sciences, Moscow, 117997, Russia; 44svnikov@mail.ru • Alexander I. Arkhipkin, Falkland Islands Government Fisheries Department, Stanley, FIQQ 1ZZ, Falkland Islands; aarkhipkin@fisheries.gov.fk Reproductive strategy is an important choice that species face continuously during their evolutionary history. A trade-off exists between fecundity and egg size (numbers vs "quality" of hatchling) because generative production in every species is restricted by body size, available food and longevity (Kasyanov 1999). Understanding these competing strategies led to the idea of r-and K-selection in life histories (MacArthur & Wilson 1967, Pianka 1970. It involves a bet-hedging concept that assumes that maximizing strategies are more advantageous in stable and predictable environments where variance is minimal, while minimizing strategies can enhance long-term fitness in periodically variable environments. Because of this, r-populations tend to inhabit unpredicta...

Ammonoid Habitats and Life History

“…After that stage, a change in ornamentation and shape occured (Currie 1942(Currie , 1944Burnaby 1966, Lehmann 1966Kulicki 1974Kulicki , 1979Kulicki , 1996Bandel et al 1982;Ward and Bandel 1987;Landman 1987, Landman et al 1996b, 2007aMaeda 1993;Kulicki and Doguzhaeva 1994;Bucher et al 1996;Doguzhaeva 2002;Kulicki et al 2002;Sprey 2002;Korn and Klug 2007;Tanabe et al 2010b). The corresponding term in nautiloids is nauta (Laptikhovsky et al 2013). According to Laptikhovsky et al (2013), the average ammonitella diameter was 0.54-2.6 mm, decreasing in mean size from the Devonian (up to > 5 mm; De Baets et al 2015) via the Carboniferous with 0.6-1.4 mm to the latest Cretaceous with 0.7-1.0 mm.…”

“…The corresponding term in nautiloids is nauta (Laptikhovsky et al 2013). According to Laptikhovsky et al (2013), the average ammonitella diameter was 0.54-2.6 mm, decreasing in mean size from the Devonian (up to > 5 mm; De Baets et al 2015) via the Carboniferous with 0.6-1.4 mm to the latest Cretaceous with 0.7-1.0 mm. Laptikhovsky et al (2013) concluded that seawater temperatures were the key factor provoking historical changes in ammonoid and nautiloid evolution.…”

“…The terminology of growth stages used herein is based on ontogenetic stages defined by numerous authors (House 1985;Kant 1975;Kullmann and Scheuch 1970, Westermann 1954Landman 1987;Kullmann 1981;Kant and Kullmann 1988;Landman 1988;Bucher et al 1996;Klug 2001;Korn and Klug 2002Etches et al 2009;Lukeneder et al 2010;De Baets et al 2012Laptikhovsky et al 2013;. The exact definition of the ontogenetic stages is crucial for reconstructing life cycles with coeval changes of habitats.…”

Ammonoid Intraspecific Variability

“…A negative relationship between egg size and environmental temperature is known from extant cephalopods and has been reported both within species and between species (e.g., Laptikhovsky 2006). Latitudinal temperature-related differences in embryonic shell size might also have been present in ammonoids (Laptikhovsky et al 2013), but so far, the fossil record is spatially too patchy to test geographic differences in contemporary populations of the same species over large latitudinal distances, where this could be relevant (Tajika and Wani 2011). In extant cephalopods, there is also a large intrinsic variation at hatching at the same locality , which might also contribute to the large intraspecific variation reported in various ammonoids sampled from restricted intervals in time and space from the Paleozoic (Erben 1950(Erben , 1964Tanabe et al 1995;Stephen and Stanton 2002) to the Mesozoic (Tanabe 1977a, b;Landman 1987;Rouget and Neige 2001;Tanabe et al 2003;Tajika and Wani 2011).…”

Bivalves from the Middle Ordovician Šárka Formation (Prague Basin, Czech Republic)

“…According to Thorson (1961) or Jablonski & Lutz (1980) about 65-70% the Recent species of bivalves have planktotrophic larvae and this type of larva permits the dispersion over the large distances. Babin (1995) and Sánchez & Babin (2003) presumed that all the Ordovician bivalves had the lecithotrophic larvae and this could explain the spatial restriction for the Ordovician bivalve genera (for early ontogenetic strategies in other molluscs, see Nützel & Frýda 2003, Manda 2008b, Klug et al 2010, Manda & Frýda 2010, Laptikhovsky et al 2013. Thorson (1961) studied the length of pelagic larval life in Recent marine invertebrates (including bivalves) and the larval transport by ocean currents.…”