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Coevolution of Post‐Palaeozoic Arthropod Basibiont Diversity and Encrusting Bryozoan Epibiont Diversity?

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Coevolution of Post‐Palaeozoic Arthropod Basibiont Diversity and Encrusting Bryozoan Epibiont Diversity? Coevolution of post‐Palaeozoic arthropod basibiont diversity and encrusting bryozoan epibiont diversity? MARCUS M. KEY JR. AND CARRIE E. SCHWEITZER Key Jr., M. M., Schweitzer, C. E. 2019: Coevolution of post‐Palaeozoic arthropod basibiont diversity and encrusting bryozoan epibiont diversity? Lethaia , Vol. 53, pp. 183–198. We hypothesize that the diversification of motile marine arthropods with hard carapaces resulted in a concurrent increase in the diversity of encrusting marine bryozoans whose larvae exploited those substrates through the Mesozoic and Cenozoic. To test this, fam- ily‐level data were tabulated from the literature on the post‐Palaeozoic diversity of motile marine arthropod basibionts and sessile marine bryozoan epibionts. We found strong temporal correlation from general to more specificbasibiont‐epibiont relationships (i.e. arthropods and bryozoans in general to decapods and encrusting gymnolaemates to robust decapods and encrusting cheilostomes in particular). We compared the diversifi- cation of bryozoans to another common group of basibionts (i.e. molluscs) and found weaker correlations. This suggests that the diversification of motile arthropods with hard carapaces (e.g. brachyuran crabs) may have played a role in the diversification of sessile bryozoans (e.g. encrusting cheilostomes) in the post‐Palaeozoic. □ Arthropoda, Bry- ozoa, Cheilostomata, Chelicerata, coevolution, epibiosis. Marcus M. Key Jr. ✉ [[email protected]], Department of Earth Sciences, Dickinson Col- lege, P.O. Box 1773, Carlisle, PA 17013, USA; Carrie E. Schweitzer [[email protected]], Department of Geology, Kent State University at Stark, 6000 Frank Avenue NW, North Canton, OH 44720, USA; manuscript received on 11/02/2019; manuscript accepted on 17/05/2019. Coevolution is the evolution of one clade in response recently developed by Gracia‐Lázaro et al. (2018). to its interaction with another clade (Janzen 1980). Their study suggests there could be a link between The study of coevolution includes a long history of increased diversity of mutualistic organisms. There- hypothesis testing with varied results (Ehrlich & fore, we hypothesize that the diversification of motile Raven 1964; Nitecki 1983; Robinson & Clark 2018). arthropods with hard carapaces should result in a One of the most studied types of coevolution is sym- concurrent increase in the diversity of encrusting biotic relationships (Futuyma & Slatkin 1983). This bryozoans whose larvae exploit those substrates. The is especially true of the concept of mutualism since mutualistic positive feedback system could work by Janzen's (1966) famous study of ants and acacia increased motile arthropod abundance triggering an plants. increase in the number of substrates for encrusting Arthropods have a rich fossil record of symbiotic bryozoans. This potentially benefits the bryozoans by relationships (Feldmann 2003a). These include epi- increasing substrate space and reducing substrate bionts such as limpets (Robin et al. 2017), barnacles competition, all while reducing predation and (Glaessner 1969) and bryozoans (Aguirre‐Urreta & increasing feeding by living on a motile host. This Olivero 1992). While tabulating diversity data on potentially benefits the arthropods by increasing arthropod basibionts and bryozoan epibionts (Sch- camouflage for the host and reducing predation weitzer & Feldmann 2015; Key et al. 2017), we (Wicksten 1979, 1993). These factors trigger an noticed a general similarity in the stratigraphical dis- increase in diversity of both arthropods and bry- tribution of decapod arthropods and cheilostome ozoans. These benefits (e.g. camouflage) and costs bryozoans. The first occurrences of brachyuran deca- (e.g. living on a moulting host) resulting from arthro- pods and encrusting cheilostomes are observed from pod‐bryozoan relationships are well reviewed by Ross the Jurassic with the majority of the diversification (1983) and Key et al. (1996a). occurring from the Late Cretaceous to the Eocene. Bryozoans are one of the most common epibionts Could this apparent simultaneous timing in diversity on arthropod exoskeletons (Ross 1983; Wahl 2009). be linked in a co‐evolutionary basibiont‐epibiont Extant motile host basibionts, like arthropods, pro- relationship? vide additional hard substrates for cheilostome bry- A multilayer network that models the positive ozoan larvae to settle (Key et al. 1995, 1996a,b, effect of mutualistic coevolution on diversity was 1999). Therefore, we hypothesize that the diversity of DOI 10.1111/let.12350 © 2019 Lethaia Foundation. Published by John Wiley & Sons Ltd 184 M. M. Key Jr. & C. E. Schweitzer LETHAIA 53 (2020) arthropods with hard carapaces and encrusting bry- Studies often use temporal correlation of time ser- ozoans should co‐vary through time. Hard substrate ies data to infer causality (e.g. anthropogenic green- space is a limiting factor for bryozoans, especially house gas emissions and global warming). Studies on encrusting bryozoans (Jackson 1977; Lidgard & Jack- arthropods (Minelli et al. 2013; Klompmaker et al. son 1989; McKinney 1995; Taylor 2016). Therefore, 2015) and bryozoans (McKinney & Jackson 1989; any increase in hard substrate space (e.g. motile host Taylor & Waeschenbach 2015) often use biodiversity basibionts) should cause an increase in bryozoan time series data to infer evolutionary causality. When diversity as documented by Balazy & Kuklinski trying to interpret biodiversity time series data, it is (2013). important to keep in mind that temporal correlation We follow the terminology of Wahl (1989) and does not necessarily imply causation (Hannisdal & refer to the motile arthropods as basibionts (i.e. the Liow 2018). The approach we take is to test for sig- host substrate organisms) and the bryozoans as epi- nificant temporal correlation from general to more bionts (i.e. the sessile organisms attached to the basi- specific basibiont‐epibiont relationships. biont's outer surface without trophically depending on it). Following the terminology of Taylor & Wilson (2002), we will focus on epibionts as opposed to Materials and methods endosymbionts as the bryozoans are ectosymbionts or episkeletozoans inhabiting the exoskeleton of their We tabulated data from the literature on the diversity host arthropod. of motile marine arthropod basibionts and marine Arthropods in general have evolved multiple sym- bryozoan epibionts through the Mesozoic and Ceno- biotic relationships (Ross 1983). Crustaceans in par- zoic. We restricted this study to the post‐Palaeozoic ticular have more symbiotic relationships than as decapod arthropods and cheilostome bryozoans perhaps any major group of invertebrates (Ross are members of Class Malacostraca and Class Gym- 1983). Symbioses occur in all major groups of crus- nolaemata which are both associated with Sepkoski's taceans, especially those with larger exoskeletons (1981, 1984) Modern Evolutionary Fauna. Members such as the isopods and decapods (Ross 1983). Of of this Modern fauna may have originated in the the marine animals, crustaceans are the most diverse Palaeozoic but their diversification did not accelerate group of basibionts and bryozoans are the most until the Mesozoic and Cenozoic. diverse group of epibionts (Wahl 2009, fig. 4.2). A Temporally, we used post‐Palaeozoic stage‐level classic example of extant decapod‐bryozoan symbio- bins except for the short stages of the Quaternary, sis includes decorator crabs using bryozoans as where we used series. When there was a disagree- masking material (Parapar et al. 1997; Stachowicz & ment in the literature about a taxon's stratigraphical Hay 2000). Basibiont‐epibiont relationships among range, we used the greater range as the fossil record fossilized decapod arthropods and cheilostome bry- more often underestimates stratigraphical ranges ozoans have been recently reviewed by Key et al. (Marshall 1990; Donoghue & Benton 2007). For a (2017). geological time scale, we used the International Com- There are some limitations in using the fossil mission on Stratigraphy's 2018/08 version of the record of arthropod‐bryozoan symbioses. First, International Chronostratigraphic Chart (Cohen et some arthropod carapaces are weakly calcified and al. 2013). We did not range families through unless not likely to be fossilized (Plotnick 1986; Hof & there were occurrences in several epochs of the Briggs 1997; Klompmaker et al. 2017). Second, some Cenozoic or if identifications were personally verified arthropods eat their exuviae following moulting as recommended by Schweitzer & Feldmann (2014, (Skinner 1985; Wolcott & Hines 1990; Swift 1992; 2015). To avoid the preservational bias of including Jernakoff et al. 1993) which reduces the chance of Modern faunas, we followed standard practice (Foote fossilization. Third, the vagaries of fossilization of & Miller 2007) and excluded the Holocene data. The the host arthropod's epicuticle makes the preserva- stage‐level bins ranged in duration from 0.70 (Ind- tion of any attached epibionts under‐represented in uan) to 18.5 Myr (Norian) (mean = 5.2 Myr, stan- the fossil record (Feldmann 2003a,b; Waugh et al. dard deviation = 3.4 Myr). To correct for this 2004). Fourth, some encrusting bryozoans lack variation, we used the number of families per million biomineralization (i.e. Order Ctenostomata) so are years for each stage in all the analyses. less common in the fossil record. Fortunately, some Taxonomically, we used family‐level data as fam- ctenostomes can etch into substrates (Pohowsky ily‐level diversity and stratigraphical range
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