The old and the new plankton: ecological replacement of associations of mollusc plankton and giant filter feeders after the Cretaceous?

Estimating ammonoid fecundity

Applying the data and calculations listed in the method section to the lectotype of Parapuzosia seppenradense, we obtain a whorl expansion rate W of 1.73 and then an according body chamber volume V_BC of 137,075,470 mm³. Depending on the proportion of the gonads (between 8 and 30%; see discussion in ‘Methods’), we obtain gonad volumes varying between about 10,000,000 mm³ and 40,000,000 mm³. Assuming an egg-volume of 1 mm³, we obtain numbers of 10,000,000 to 40,000,000 eggs per adult female Parapuzosia seppenradensis (see also Fig. 2) if they were semelparous. If we assume iteroparity, these numbers increase by the factor of the number of reproductive cycles. Also, if we assume that the eggs and embryos continued to grow after they were laid (see discussion in Walton, Korn & Klug, 2010), ammonoid fecundity would further increase, but evidence for this is missing in ammonoids (Mironenko & Rogov, 2016). For an adult female of half the diameter, we would still obtain egg-numbers of between 3,000,000 (8% gonad volume) and 10,000,000 eggs (30% gonad volume) at semelparity. Puzosiids and other large Cretaceous ammonoids in the size range between 500 and 1,000 mm are quite common worldwide (e.g., Pachydesmoceras).

In Fig. 2, we depict the relationship between the number of eggs per female adult ammonoid using mostly published data and the results presented here. The loglog-biplot shows an exponential relationship between these two parameters, which is not surprising taking into account how the estimates were achieved (De Baets et al., 2012). It also shows some variation scattering around the exponential trend line, which likely roots in the variation of the ratio of embryonic versus adult conch size (e.g., Gyroceratites and Sinzovia have similar adult sizes, but the embryonic conch is 50% larger in Gyroceratites; De Baets et al., 2012; De Baets, Landman & Tanabe, 2015; Mironenko & Rogov, 2016).

The role of r-strategy in ammonite and belemnite ecology

Depending on the proportional gonad size and whether or not ammonites were semelparous or iteroparous, it appears likely that adult females of the largest puzosiid ammonites such as Parapuzosia seppenradensis laid between 10,000,000 and 100,000,000 eggs and ammonoids about half the size still over 1,000,000 eggs. The simple calculation above highlights the likelihood that derived ammonites were extreme r-strategists (respectively fast life strategy), which produced vast amounts of offspring, likely contributing an important part of the plankton in size at the limit from micro- to macroplankton. R-strategy corresponded with high mortality and it is likely that hatchlings and juveniles of ammonites formed a major source of food in the marine realm.

As far as belemnites are concerned, their global abundance had already decreased during the Late Cretaceous (prior to the main extinction event), freeing ecospace for, e.g., some other coleoids (Iba et al., 2011). Nevertheless, coleoids with conical phragmocones such as belemnites, diplobelids, Groenlandibelus or Naefia share a small initial chamber and likely small embryonic conchs (Bandel et al., 1984). Above all, there are a lot of similarities between belemnite and ammonite hatchlings such as their small initial chambers, their overall hatchling size, their supposed habitats including the planktonic mode of life and the r-strategy reproductive mode (Ward & Bandel, 1987; Arkhipkin & Laptikhovsky, 2012; Doguzhaeva et al., 2014). Accordingly, we assume that belemnite fecundity was also high, although much lower than those of the puzosiid ammonites because of the much lower size difference between adults and embryos (about 100–1,000 eggs per female).

Which animals ate ammonites?

Evidence for successful and unsuccessful predation on medium to large-sized ammonites is not rare but identifying the actual predator is possible only in very few cases (Keupp, 2012; Hoffmann & Keupp, 2015). Additionally, most hard parts of ammonites (conch and lower jaw) were likely crushed by the predators and quickly dissolved in the digestive tract, making ammonites as fossilized stomach contents improbable, although a few cases have been reported where juvenile ammonoid remains are preserved in stomachs of Jurassic ammonites (Keupp & Schweigert, 2015; Klug & Lehmann, 2015). It is even more difficult to find evidence for predators that fed on hatchlings and neanic juveniles of ammonites (dm < 10 mm), which must have occurred in vast numbers in the world’s oceans of the Mesozoic. These early post-hatching developmental stages probably lived in the water column because their conchs already had functional phragmocones and they are often found in black shales, which were deposited under hypoxic to anoxic bottom water conditions and therefore, a strictly benthic mode of life was impossible (Shigeta, 1993; Nützel & Mapes, 2001; Mapes & Nützel, 2009). Thus, pelagic nektonic animals (including older growth stages of ammonites) are the likeliest candidates as predators feeding on these young ammonites: Fig. 3 depicts the fitting of juvenile planktonic ammonites and holoplanktonic gastropods with the mesh size of filter feeders of the corresponding time intervals. See Fig. 4 for the stratigraphic distribution of the groups discussed here.

For abundant and easy prey like juvenile ammonites, a broad range of predators can be hypothesized. Like plankton today, these masses of juvenile ammonites represent perfect food sources for medium-sized to large suspension feeders (invertebrates and vertebrates). From the Cretaceous, giant planktivorous bony fishes (pachycormids: Friedman et al., 2010) have been suggested to be nektonic suspension feeders, which might have fed on plankton comprising a wealth of juvenile ammonites. In the SOM of their paper, Friedman et al. (2010) show a fragment of the gill rakers; their filaments have a spacing of about 1 mm, which is suitable to filter out hatchlings and juvenile ammonites with conchs of one millimeter in diameter or slightly more (Fig. 3). This trophic relationship is further suggested by the extinction of this group synchronous with the demise of the Ammonoidea and Belemnitida but direct evidence is missing. Taking the direct fossil evidence from the Jurassic into account, it appears likely that ammonites also played a role as micropredators feeding on early juvenile ammonite offspring (Jäger & Fraaye, 1997; Klug & Lehmann, 2015; Keupp, 2012; Kruta et al., 2011; Keupp & Schweigert, 2015; Keupp et al., 2016).

The extreme differences in size (up to three orders in magnitude) between adults and juveniles in large ammonites indicate that the range of potential predators changed significantly throughout the life history of these cephalopods. As hatchlings and small juvenile planktonic forms, moderate-sized to large suspension feeders and small predators likely used them as a food source but for adult puzosiids and other large ammonites, only large predators such as mosasaurs, pliosaurs and large fishes can be considered, although the seeming direct evidence for such a trophic relationship is still under debate (Kauffman & Kesling, 1960; Tsujita & Westermann, 2001; Kauffman, 2004; Gale, Kennedy & Martill, 2017). Latest Cretaceous juvenile ammonites were possibly not the primary food source of ichthyosaurs since the latter became extinct already in the Cenomanian and are unknown from stomach contents to our knowledge. After the demise of ichthyosaurs, ammonites persisted to be diverse and abundant. In spite of a better link of their extinction with that of the belemnites in the North Pacific near the end of the Early Cretaceous (Iba et al., 2011), belemnite decline in the Tethys at the Cenomanian–Turonian boundary (Doyle, 1992; Christensen, 2002) and direct evidence for a trophic relationship between phragmocone-bearing coleoids and ichthyosaurs (Kear, Briggs & Donovan, 1995 and references therein), Acikkol (2015) suggested that a link between the severe reduction of belemnite diversity and ichthyosaur extinction is unlikely.

An additional point we want to raise is the role of adult ammonites as micropredators feeding on juvenile ammonites. It has been claimed by various authors that ammonites, particularly heteromorphs, lived in the water column (Cecca, 1997; Guex, 2006), i.e., with direct access to meso- and microplankton. As pointed out above, a microphagous diet has been shown for several ammonite species including heteromorphs (Jäger & Fraaye, 1997; Klug & Lehmann, 2015; Keupp, 2012; Kruta et al., 2011; Keupp & Schweigert, 2015; Keupp et al., 2016), thus making ammonites as predators feeding on juvenile ammonites in the Cretaceous likely.

Which groups filled the ecospace freed by the extinction of ammonite hatchlings and planktivorous actinopterygians?

Association of the extinctions of large marine reptiles, large planktivorous fish and those of ammonites and belemnites suggest trophic relationships between these groups; their extinction freed ecospace for both small zooplankton and various suspension feeders as well as predators. This association is followed by major changes in the planktonic realm such as the rise of holoplanktonic gastropods. Although a few Early Jurassic to Cretaceous heteropods are known (Bandel & Hemleben, 1995; Nützel, 2014; Teichert & Nützel, 2015; Janssen & Goedert, 2016; Nützel et al., 2016; Burridge et al., 2017; Janssen & Peijnenburg, 2017), the major expansion of heteropods and ‘pteropods’ falls into the Cenozoic (Lalli & Gilmer, 1989; Tracey, Todd & Erwin, 1993; Janssen & Goedert, 2016; Janssen & Peijnenburg, 2013).

In size and their coiled form, many fossil Limacinidae (Thecosomata, planktonic opisthobranch gastropods) resemble ammonites. Similarly, the conchs of fossil Creseidae morphologically and in size (at least roughly) correspond to hatchlings of belemnites, diplobelids and other phragmocone-bearing coleoids of the Cretaceous (Bandel et al., 1984; Lokho & Kumar, 2008). In addition to these morphologic similarities, these groups shared the planktonic habitat. According to Janssen & King (1988), Janssen & Peijnenburg (1988), ‘pteropods’ were already present at least as early as the latest Palaeocene (see also Janssen & Goedert, 2016). Janssen & Goedert (2016) even claimed a Cretaceous origin of the Thecosomata. A number of Eocene pteropod occurrences are known worldwide (Bristow, Ellison & Wood, 1980; King, 1981; Curry, 1982; Zorn, 1991; Hodgkinson, Garvie & Bé, 1992; Janssen, Schnetler & Heilmann-Clausen, 2007; Lokho & Kumar, 2008; Ando, Ujihara & Ichihara, 2009; Cahuzac & Janssen, 2010). An early Palaeogene origin is also supported by a combination of palaeontological and molecular clock data published by Corse et al. (2013). Remarkably, the latter authors compare the uncoiling of the conch of Thecosomata with the coiling of ammonites, but they did not discuss macroecological implications such as the ecological replacements suggested here. As far as abundance of these fossils is concerned, pteropods are much less frequent than subadult to adult ammonites and belemnites, while their hatchlings are similarly rare. This is probably due to the combination of their small body size as well as their thin and fragile aragonitic shells (Janssen & King, 1988), which did not provide a high fossilization potential. The great majority of these thin aragonitic shells was undoubtedly rapidly dissolved during early diagenesis and as a consequence not fossilized (Berner, 1977; Janssen & Peijnenburg, 2017). Nevertheless, the fact that numerous pteropods have been reported from the Eocene implies that they were abundant and widely distributed at least since that period of time.

Similarities in size, overall morphology, habitat, abundance as well as the timing of their respective extinction and origination suggest that hatchlings and small individuals of ammonites as well as belemnites were ecologically replaced, at least partially, by planktonic opisthobranchs (Thecosomata) and other holoplanktonic gastropods. In turn, the ecological installation of the Thecosomata together with other planktonic organisms contributed to the dietary basis for the evolution of new groups of large planktivorous suspension feeders (Lalli & Gilmer, 1989; Armstrong et al., 2005; Hunt et al., 2008). As suggested by Friedman et al. (2010), the Cretaceous ‘giant planktivorous bony fishes’ found an ecological replacement in both large suspension-feeding chondrichthyans and baleen whales. Several of these groups are known to take in important amounts of planktonic gastropods, although arthropods such as krill and other plankton plays important roles as well. Today, thecosomes may regionally contribute up to 50% of the zooplanktonic biomass and thus are ecologically important (Mackas & Galbraith, 2012). However, today’s Manta rays (Mobulidae) are known to feed predominantly on small Crustaceans, small fish and other plankton and the same holds true for several baleen whales (e.g. Sims & Merrett, 1997; Motta et al., 2010; De la Parra Venegas et al., 2011; Slater et al., 2017). Nevertheless, it is unknown what exactly these Palaeogene suspension feeders ate, but at least the filter mesh spacing of both planktivorous chondrichthyans and several baleen whales fits well with the size range of thecosomes (Fig. 3). Also, it is conceivable that early filter feeding species of these groups did not discriminate in their planktonic diet as much as more derived modern relatives. In any case, the niche of filterers catching prey of a size of a few millimetres was occupied by the chondrichthyan and marine mammal filter feeders mentioned above. The Thecosomata can thus be understood as an example for the new plankton that occurred after the end-Cretaceous mass extinction.

What caused this ecological replacement?

The fossil record comprises quite a few cases of ecological replacements (which are often called ‘biotic replacements’; e.g., Benton, 1987; Benton, 1991; Briggs, 1998). Some famous examples include replacements of brachiopods by bivalves (Gould & Calloway, 1980; Payne et al., 2014), dinosaurs by mammals (e.g., Sloan et al., 1986), hybodonts by modern sharks (Schaeffer, 1965), and ‘straight-necked’ turtles by ‘flexible-neck’ turtles (Rosenzweig & McCord, 1991; for a comprehensive list of ecological replacement, see Benton, 1987; Benton, 1991). These examples are also used to discuss possible mechanisms, which explain what drove the replacement and in turn, facilitated speciation or macroevolution of clades. Benton (1991) presented several models of ecological replacements, in which the role of competition, key adaptation and mass extinction was discussed as main cause of such replacements. He concluded that ‘competition’ and ‘key adaptation’ can rarely be the main cause of such replacements, although the role of mass extinction also needs to be further examined. By contrast, some other researchers have different views on mechanisms of ecological replacements. For instance, Rosenzweig & McCord (1991) wrote the following: “species from the new clade produce new species to replace already extinct species from the old clade. The key adaptation gives them a higher competitive speciation rate than old-clade sources of replacement”. They presented the example of the straight-necked turtles (Amphichelydia), which were replaced by cryptodiran turtles with the capability of neck retraction and termed this model of replacement ‘incumbent replacement’. In this mechanism, key adaptations play a major role. Also, Briggs (1998) argued that several cases of ecological replacement, which are cited as evidence for mass-extinction-induced replacements, took place over a long period of time, and thus, biological interaction played a primary role.

In the case of ammonoids and belemnites being ecologically replaced by holoplanktonic gastropods, it partially depends on the phylogenetic and temporal scale that is examined and on the fossil record. When focusing only on ammonoids and belemnites, no species remained after the Cretaceous to compete with Palaeogene holoplanktonic gastropods. By contrast, when including the whole clade, this looks different since cephalopods continued to exist and gastropods were also present long before this faunal change (Fig. 5; Sepkoski, 1981). What makes this more relevant is the end-Cretaceous diversity reduction among the Cephalopoda in a phase where the whole clade Gastropoda diversified (a longterm process that started already in the Triassic, which was largely a result of the expansion of Neogastropda). Naturally, both Cephalopoda and Gastropoda contain species with a broad range of different modes of life and thus, their differing diversity patterns cannot be explained by the ecological replacement of juvenile ammonites by holoplanktonic gastropods alone—especially although holoplanktonic gastropods are abundant and widely distributed, their diversity is not high. On the other hand, the removal of ammonites and belemnites from the planktonic realm offered certain gastropods the opportunity to flourish in this realm and to long for new opportunities including availability of food and space resources.

As far as key adaptations (e.g., Simpson, 1943; Benton, 1983; Benton, 1987; Rosenzweig & McCord, 1991; Briggs, 1998; Payne et al., 2014) are concerned, they were already present in the group of species assuming the ecological role of the previously incumbent species after their extinction (Rosenzweig & McCord, 1991). Although some researchers report the presence of holoplanktonic gastropods in the Cretaceous (Janssen & Goedert, 2016; Burridge et al., 2017), to date, there is no fossil evidence, which suggests that they acquired all key adaptations that ensured the success of radiation in the Cenozoic except the small, thin-shelled conch. Also, due to a lack of data, it is not possible yet to conclude whether or not a direct biotic interaction between the old (ammonite and belemnite hatchlings) and the new (holoplanktonic gastropods) clades occurred in the Cretaceous, although the Thecosomata originated already in the late Campanian (Janssen & Goedert, 2016; Burridge et al., 2017). At least, the fossil record suggests that this case of replacement was triggered by a mass extinction event. In Fig. 6, we show the distribution of sizes of embryonic conchs of ammonites compared to the earliest occurrences of Thecosomata in the fossil record demonstrating the size-overlap between the two groups. Moreover, the evolution of a holoplanktonic mode of life is particularly easy in gastropods with a planktotrophic veliger larva. Bandel et al. (1984) have convincingly shown that pteropods evolved through neotenic extension of larval life of a benthic ancestor. A similar model has been proposed by Teichert & Nützel (2015) for Jurassic heteropods, which are superabundant in the Early Jurassic Posidonia Shale. Here, repeated Early Jurassic Anoxia resulted in neotenic prolongation of larval life to a holoplanktonic adult life. Thus, the free-swimming veliger larvae may be seen as an preadaptation for a holoplanktonic mode of life in these gastropods and this way the timely overlap that is required for in the incumbency model applies.

Nevertheless, the main radiation of the Thecosomata appears delayed until the Palaeocene-Eocene boundary judging from their fossil record (Janssen, Schnetler & Heilmann-Clausen, 2007; Janssen & Peijnenburg, 2017). This raises the question whether this delay in radiation is an artefact of the poor fossil record of the Thecosomata or whether the main radiation really occurred several million years after the Cretaceous. Considering that a species loss caused by a mass extinction event can require as long as 5–10 My for community recovery (Copper, 1989), it appears likely that the radiation of holoplanktonic gastropods began in the Palaeocene. It must be taken into account that adaptation to the new life style including optimization of resource exploitation needed time.

Although we cannot rule out key adaptations and biotic interaction as main causes of the ecological exchange of ammonites and belemnites by Thecosomata and other holoplantonic gastropods after the Cretaceous, it is probably safe to claim that the holoplanktonic gastropods opportunistically benefited from the ecospace vacated by the extinction of these two groups of cephalopods. Possibly, new finds of holoplanktonic gastropods from the early Palaeocene will push their radiation back in time closer to the extinction of ammonoids.