Parasitic flowering plant collections embody the extended specimen

Natural history collections underpin most biodiversity investigations, serving as crucial resources for species identification, taxonomy, biogeography and evolutionary (Heberling et al., 2019; Meineke, Davies, 2019). These are also critical education promotion of inquiry-based training active learning (Lacey 2017; Powers 2014). well-established common applications natural have, in recent decades, been complemented by a variety new approaches facilitated technological advances, including next generation sequencing isotope analysis, well extensive efforts specimen digitization online data sharing (Hedrick 2020; Hilton 2021; Meineke 2018; Nelson & Ellis, As result these developments, studies realms such functional ecology, ecological modelling, phenology, morphometrics have greatly stimulated the increasing availability big captured from specimens (Heberling, 2022; Hedrick Monfils 2017). The ongoing revolution application cutting edge timely research is framed concept ‘extended specimen’. Proposed Webster (2017), idea represents totality types associated with specimen, frequently overlooked streams, which together provide broader view individual's extended phenotype. This framework great motivator deeper exploration via innovative preparations analyses (Lendemer 2020). In particular, practice ‘holistic sampling’ builds on advocating collection analysis closely symbionts addition to focal species, parasites/hosts, that preserved but (Schindel Cook, 2018). fact, ‘extend’ main preserving curating its not only optimize sampling efforts, potential promote interdisciplinary (Thompson 2021). inherently contain multispecies relationships, lichens, certain parasites fungi, we suggest parasitic plant serve key examples development specimen. From parasite (Figure 1a), first extension digitization, digital image record Secondary extensions relate molecular, isotopic chemical data, anatomical, phenological environmental information about symbiont(s) 1b). further enable tertiary extensions, stimulating areas like biogeography, distribution, modelling ecology hosts 1c). Here, use an iconic ideal representation Extended Specimen example can be expanded many other capture interactions. Our focus ‘specimen extensions’ warranted fact parasitism form symbiosis feeding modality; indeed, all organisms engage relationships at some level being either and/or (Combes, 2001). interactions essential biodiversity, ecosystem functioning processes. Specifically, repeatedly shown modulate intraspecific competition, community composition, migration local abundance both host non-host thereby providing services 1996; Frainer Karvonen Seehausen, 2012; Phoenix Press, 2005). face continued global change, expected play even greater role dynamics, leading cascade potentially community-wide effects may outweigh direct change upon single (Gilman 2010). For instance, depend intermediary or mutualistic complete their life cycles; increased temperatures cause mismatches among thus aiding accelerated evolution resistance populations (Mateos-Gonzalez 2015) restricting future distributions (Ornelas turn, changes distribution modify outcome triggering instability 1996). At same time, conservation biology demonstrates extinction risk vulnerable impacts due climate indirect through coextinction (Carlson 2017, Thus, especially important understanding complex biological systems over broad spatial temporal scales (Brooks Hoberg, 2007; Harmon case zoonotic parasites, hindered poor relative taxa, lack vouchered curatorial difficulties (Bell Thompson On hand, wealth already available seldom explored context (Andrew angiosperm herbaria, despite attracting phylogenetics remain ignored general discussions integrative research. With interest novel collections, now time light. lifestyle has evolved multiple times within land plants, involving least two different modes resource acquisition (Heide-Jørgensen, 2013). A mode includes mycoheterotrophic adopted procurement nutrients mycorrhizal fungal intermediaries (Merckx 2009). contrast, more specialized nutritional depends haustorium, hybrid root–shoot organ acts living bridge, connecting plants (Teixeira-Costa, haustorial this review, penetrate physically attached haustorium initial stages onwards. Shortly after penetration, vascular connection established between allowing water uptake parasite, bilateral exchange hormones, proteins genetic material (Yoshida 2016). highly organ, coupled it, wide histories, specificities, morphological traits eco-physiological attributes (Teixeira-Costa Davis, peculiar characteristics long attention naturalists collectors. Perhaps surprisingly, known herbarium modern (Stefanaki diversity mirrored network interdependencies they form, goes far beyond include pollinators, seed dispersers, herbivores pathogens (Watson Herring, 2012). Field demonstrated might extend impact plant, animal indirectly (Cullings 2005; Hartley 2015; Spasojevic Suding, 2011). It noteworthy while ecologically interconnected pollinators trophic levels associated, invertebrate microbes. reason, disproportionally large effect modulating structure function, urban areas, often considered keystone (Phoenix context, represent ‘information hubs’ swath secondary 1, sensu Lendemer 2020) gathered applied ranging co-evolutionary dynamics macro-ecology plasticity directly 2). Global benefit well-curated richness preserve. review how represented records. We then discuss various ways understand scales. Finally, comment best practices field, subsequently preparing digitizing specimens. account taxonomic recognizes nearly 5,000 classified 12 distinct clades constituting c. 1.6% extant (Nickrent, Teixeira-Costa number distributed across continents (except Antarctica) several remote islands, spanning terrestrial biomes, deserts high arctic 2013; Owing major collections. Although vast majority 396+ million than 3,000 herbaria globally (Thiers, 2021) yet digitized mobilized online, significant records aggregators enabling large, synthetic addressing basic questions ideas Isaac, Soltis, To stimulate using specimens, present overview around globe biases guide priorities efforts. accomplish our goal, were obtained Biodiversity Information Facility (GBIF.org, 2021: https://doi.org/10.15468/dl.dpsg3s). dataset was initially filtered exclude without identity below family (e.g. genus species), no institutional provenance cases when field ‘institution code’ empty, attempt made obtain analysing fields, namely ‘collection code’, ‘catalogue number’, ‘record number’ ‘rights holder’. Collections belonging institution grouped under code A, AMES, ECON, FH, GH NEBC ‘HUH’—Harvard University Herbaria). total 1,017,028 included final (Table 1). Considering currently recognized flowering 2021), overall GBIF results average 206 specimens/species. ratio vastly surpasses representing symbiotic associations, indicating collected category plants. Parasitic animals protozoans, estimated massive 3.5 (Dobson 2008; Mora 2011) ~2.8 lots Nevertheless, observe uniformly distributed: 11.6% absent partially explained unresolved issues taxonomically genera, Orobanchaceae (Robart Tank Olmstead, 2009; Yu Differences institutions likely absence under-representation analysed data. become world-wide will better what strengths, biases, gaps exist (Nelson Most belong (53.7%; Table 1), cosmopolitan clade occur latitude coast Greenland 2013, Santalales, largest functionally diverse 32% less compared difference could that, GBIF, 98 Santalales (due insufficient funding staffing, etc.) differences. Furthermore, because annual perennial herbs, comparatively easier required collect samples trees aerial shrubs (i.e. mistletoes) comprise bulk Santalales. pronounced tropical (Santalales) versus temperate (Orobanchaceae) groups help explain Another interesting comparison composed exclusively endoparasites Apodanthaceae, Cytinaceae, Mitrastemonaceae Rafflesiaceae). Species four families independently strategy similar biotrophic is, growing incognito becoming visible human eye during short reproductive phases (Thorogood similarly restricted rare (Burgoyne, 2006; Hidayati 2000; Mir Rafflesiaceae, three endoparasite combined one lineages GBIF. Rafflesiaceae famous developing world's flowers (Nikolov 2017), publicly related creating adequate vouchers cumbersome (some spirit). Within each clade, abundant house cases, wider geographic ranges surprisingly clade. Hydnoraceae Krameriaceae notable exceptions; here, widespread example, Hydnora johannis Becc. (Hydnoraceae), central northeast Africa (Musselman Visser, 1989), Krameria tomentosa A. St.-Hil. (Krameriaceae), Brazil parts Bolivia (Simpson, 3% 13% respective instances reflect (H. africana Thunb., K. erecta Willd., Krameriaceae) close larger well-known collecting bias (Daru Musselman 1989; Simpson, 1989). unsurprising per derived Muséum National d'Histoire Naturelle (France), New York Botanical Garden (USA), Missouri Smithsonian Institution Naturalis (Netherlands), world earliest adopters industrial-scale Digitized alone 250,000 records, 25% analysed. trend observed five families, whose collectively distributions. Hydnoraceae, Krameriaceae, Lennoaceae Mitrastemonaceae, held medium-sized 2 institutions, those 5 does allow us analyse comprehensive herbarium, nor chosen prioritize digitize. observations phylogenetic investigation, contribute valuable vary according distribution. small hundred thousand unique overtime, regional holdings strong (Marsico Many small, partly so, hold light boxes lens reflex cameras flatbed scanners designed rapid imaging standard methods LED banks, camera stands mirrorless interchangeable-lens offer lower cost solutions smaller (Davis Takano long-term storage high-resolution images contributes substantially archiving calling infrastructural support truly additionally quantified georeferenced clades, 40% 3). Cynomoriaceae proportion imaged (50.3%; 515 29% (France) entire herbaria. Cynomoriaceae, Cuscuta, showed (c. each; Apart widely groups, geographical coordinates percentage line reported networks (Barkworth Murrell, 2012), above Carlson delineation, classification conducted 1; Heberling Along lines, patterns parasite–host co-evolution Bellot Renner, Previously published systematics served baseline interpreting events parasites. investigation offers window into relatively utilized 2a). Recently, Bellis al. (2020) compiled Striga hermonthica (Delile) Benth. (Orobanchaceae), noting species. Because few material, infested label (E. Bellis, pers. comm.). simultaneous creation models, genome-wide association revealing maintenance genes smallholder agroecosystems agricultural settings (Bellis findings implications human-modified landscapes investigations. relevant considering S. causes devastating food crops (Spallek 2013) adaptability independency farming scenarios uncertain (Cohn containing regarding aspects relationships. generally purpose, increasingly sources 2022), used investigate symbioses (Meineke Despite importance trait scarcely measured poorly understood Given strategies carbon, nutrients, water), it exhibit combinations dissimilar non-parasitic counterparts. Haynes (2022) recently database compare values asking whether former followed pattern coordinated variation leaf economics spectrum; Wright 2004). Interestingly, study did find evidence deviate fundamentally trends found free However, accounted 1% observations, rendering conclusions preliminary. physiology, function traits, strategy. Herbarium suggested variations (Woodward, 1987). widespread, regarded repositories 2022). propose phylogeny, space 2b). Mistletoes, particularly sensitive prolonged drought, eco-physiology insights consequences (Fontúrbel, nitrogen carbon metabolism positively correlated mistletoes (Scalon Wright, 2015), proxy inferences other. incomplete material) eco-physiology. if collection, area. Results investigations bridge knowledge vice-versa. range outcomes reveal species' phenotypic 2c). One question attracted renewed phenology associations (Rafferty 2015). utilization emerged area decades labels dates flowering, fruiting, leaf-out) underutilized, powerful phylogeny. Connecting specimen-derived historical provides insight herbivores, dispersers respond change. true Indeed, flowering/fruiting affect host-associated reward production sympatric influence vectors (Yule Bronstein, Data hypothesis co-occurring show complementary extends period flower/fruit Moreover, crosstalk mobile elements hormones regulate timing (Shen 2020), amplify communities. influences antagonist organisms, insect herbivores. Experiments elucidate tripartite differences terpenoid performance (Marvier, 1996, 1998). drivers, concentration dioxide, ozone oxides, alter biosynthesis, composition metabolites, turn plant–herbivore (Jamieson suited (Meineke, Classen, technical volatile metabolites overcome, (Foutami specific discussed quantifying herbivory profiles itself, 2d). purposes large-scale systematic (Muñoz-Rodríguez 2019) assessments hotspots (Lahaye 2008). Herbariomic approaches, however, underutilized exploring obvious utility untangling cryptic anticipate DNA barcoding facilitate identification degree confidence 2e). useful where unknown features complicated taxonomy (Pelser dynamic shifts (Schneider eDNA monitoring determine existence concern given area, hidden body (Osathanunkul, Similar identify genotypes emerging concerns (Barkman ‘extensions’ previous section involve regardless presence o