The Pierpaoli’s Herbarium MBMP: A Historical Window into Marine Biodiversity of the Ionian Sea

Abstract

Herbaria, originally books of medicinal plants, became collections of dried plants after 1500, later extending to seaweeds and supporting taxonomy and systematics. Digitalization has made herbaria accessible, and advances in DNA sequencing have transformed them into valuable resources for genetic research. Label data, which include place and date of collection, make exsiccata essential tools for biogeographic studies and conservation strategies, helping map biodiversity and protect endangered species. The historical Pierpaoli herbarium (MBMP) houses 584 seaweed specimens collected from the Ionian and Adriatic seas between 1920 and 1965. It has been digitized within the NPRR Project ITINERIS and the DiSSCo infrastructure. Floristic changes in the Mar Piccolo over three periods (1920–2024) and the Mar Grande (1920–1992) were compared using herbarium specimens, papers, and recent data. Mar Piccolo’s flora over a century revealed significant changes. Many historical species disappeared, while new ones appeared, including 14 non-indigenous species. The biogeographical composition also shifted, with Cosmopolitan and Indo-Pacific elements increasing. In the Mar Grande, less than half the species were found again in 1992. Evidently, phytobenthic communities underwent noticeable changes over a century, highlighting the impact of environmental shifts. This confirms that Natural Science Collections are invaluable resources for understanding our planet’s biodiversity and history.

1. Introduction

Herbaria, originally created as means of preserving and transmitting knowledge about the plants, date back to ancient times. They consisted of books reporting descriptions and, often, images of plants, mainly those used in the pharmacopeia due to their chemical content with medical properties. Only after 1500 did herbaria become collections of dried plants (horti sicci) when those were studied in all their aspects and their distinctive characteristics, even independently of pharmacological properties [1]. Several herbaria also included dry specimens of seaweeds over the years (e.g., Italian Central Herbarium at Florence; Muséum National d’Histoire Naturelle Herbarium at Paris, Lund University Herbarium, Natural History Museum at Milan) (https://sweetgum.nybg.org/science/ih, accessed on 31 July 2025). Among the 78 Italian herbaria, 38 preserve specimens of seaweeds, and among them, the last 4 are historical herbaria [2].

From Linnaeus (1707–1778) onwards, the primary role of herbaria has been to support the fields of taxonomy and systematics. The dried plant specimens, often called “vouchers,” have served as essential reference materials. These physical records allowed researchers to verify species identification, establish standards, and aid in new discoveries. Indeed, by comparing an unknown plant with a known voucher specimen, botanists could confidently identify similar-looking plants. Moreover, vouchers acted as a definitive standard for a species, particularly for “type specimens” used to officially name and describe a new species. This ensured consistency and accuracy in botanical nomenclature. Nevertheless, researchers would use these collections as a foundational resource when describing new species, helping them to confirm that their discovery was indeed distinct from all previously documented plants [3]. Basically, these collections were and continue to be the foundational library for plant identification and classification, providing a tangible record of Earth’s plant diversity. The considerable increase in the number of publications in this field, recorded in the last ninety years, further supports the scientific importance of herbaria [3], even though for a long period, starting in the second half of ’90s, the attention to molecular biology for plant and seaweed taxonomy studies became preponderant [4,5]. DNA extraction methods have significantly advanced, enabling the application of Next-Generation Sequencing (NGS) techniques to herbarium specimens. This is a notable development because herbaria, traditionally used for morphological studies, are now becoming valuable resources for genetic research [6,7]. However, a new interest in herbaria arose in the XXI century, also thanks to many books published even by non-experts, in which herbaria were seen in a new light [8]. A significant impulse to the scientific recovery of herbaria has arisen from their digitization, which made these repositories open access resources for all scientists [9]. Being accompanied by a label [10] and by the most recent Minimum Information about a Digital Specimen (MIDS) [11], which provides information as important as the preserved organisms themselves, such as the collection site and date, herbarium specimens serve as tangible proof of a species’ existence at a specific place and time; therefore, every herbarium is a knowledge base for biodiversity in that it provides a comprehensive checklist for a given region [6]. For this reason, researchers can also use herbaria for biogeographical purposes, mapping where species live. Such maps are extremely precious to document the change in biodiversity and to develop conservation strategies, in that they allow scientists to detect which species disappeared and which are threatened by habitat loss due to anthropic impact, as well as which species are relatively safe. Therefore, the rich data contained within herbaria have made them an essential tool for environmental sustainability in recent years, enabling new avenues of research that were previously unexplored [12].

It is known that seaweeds are excellent recorders of environmental changes, which are shown by the disappearance of some species and/or the finding of others (e.g., NIS—Non-Indigenous Species), the increase or decrease in their biomass, and shifts in depth ranges [13,14]. Recently, more and more studies have aimed to identify the nature of such changes and, possibly, quantify their magnitude. However, there are very few cases in which it was possible to verify the modification of algal flora after a period of many decades. Such studies were typically based on the comparison of macroalgal floristic lists from different times, as well as herbarium sheets [15,16,17,18,19,20]. Obviously, in such cases, the historical identifications of the species were trusted to validate the comparison of results.

One of the Italian historical seaweed herbarium is the Irma Pierpaoli’s herbarium MBMP (https://sweetgum.nybg.org/science/ih/herbarium-details/?irn=266083, accessed on 31 July 2025). It dates back to the early 1920s; it underwent a former revision at the end of 1960s by Attilio Solazzi and a latter careful nomenclatural revision in the late 1990s [21,22]. Since within the framework of the project ITINERIS, funded by the NPRR, digitization has been performed and a new nomenclatural update has occurred. The herbarium MBMP has considerable scientific importance because seaweeds were collected in restricted areas of the Ionian Sea and the Adriatic Sea, both suffering from strong environmental changes over the years. Here, we compare the flora present in the 1920s and those found in the late 1980s [23], and, more recently [20,24], in the seas of Taranto, to assess biodiversity changes and correlate them with environmental changes. Moreover, the deepening of some taxonomic questions is discussed as well as the possible detection of particular functional traits in some species.

2. Materials and Methods

2.1. Irma Pierpaoli

Irma Pierpaoli (Roma, 1891—Senigallia, 1967) was an Italian phycologist, responsible for the first in-depth studies on the benthic macroflora of the Mar Piccolo and the Mar Grande of Taranto (Ionian Sea, southern Italy) (Figure 1). She carried these studies between 1920 and 1925, when she taught at the Technical Institute “Pitagora” in Taranto and was a guest at the State Institute of Marine Biology now Istituto Talassografico “A. Cerruti”—CNR [25]. Successively, she moved to Senigallia, near Ancona (Adriatic Sea, central Italy), where she studied the seaweeds of that stretch of the Adriatic coast [22,26,27]. She has been mentioned in two monographs [25,28], in the Treccani encyclopedia [29], on the website of the University of Bologna hosting the biographical dictionary of Italian female scientists (http://scienzaa2voci.unibo.it/, accessed on 30 July 2025), and in Wikipedia, the free encyclopedia (https://it.wikipedia.org/wiki/Irma_Pierpaoli, accessed on 30 July 2025).

2.2. MBMP Herbarium

The exiccata of the specimens that Irma Pierpaoli collected from 1920 to 1965 constitute the important herbarium MBMP bearing her name, which consists of 424 sheets for a total of 584 specimens, since a sheet occasionally holds more than one thallus. Often, dry specimens are bundled with a sketch of their reproductive traits (e.g., cystocarps, sporangia) (Figure 2). In total, 72 species of Rhodophyta are preserved on 196 sheets for a total of 281 specimens, 39 species of Chlorophyta are preserved on 96 sheets for a total of 139 specimens, and 29 species of Heterokontophyta (Phaeophyceae) are preserved on 132 sheets and a total of 164 specimens. In total, 81 species were collected in the high Ionian Sea (in both the Mar Piccolo and Mar Grande basin) and 95 in the middle Adriatic. Currently, the MBMP herbarium has been digitized within the framework of the NPRR Project ITINERIS and the infrastructure DiSSCo. The digitization process involved several steps: labeling, scanning, and adding metadata to each sheet in order to create digitized specimens that meet the first or second level of MIDS [30]

2.3. Assessment of Biodiversity Changes

Concerning the assessment of changes in floristic composition that occurred in the Mar Piccolo over the past century (Figure 1), a comparison was made among the floristic lists of the following three periods: 1920–1925 (I hereinafter), obtained from both herbarium MBMP samples and papers [31,32,33]; 1986–1992 (II hereinafter) [23,34]; and 2011–2024 (III hereinafter) [20,24] (A. Petrocelli unpublished data). The analysis also included an assessment of the biogeographic element for each listed species. As for the Mar Grande basin (Figure 1), in order to enable a comparison with more recent data, the complete list of species collected by Irma Pierpaoli at S. Nicolicchio rock was obtained by examining both the herbarium MBMP and her papers [31,33]. After updating the nomenclature, the list was compared with data derived from samplings carried out in May and October 1992 along the coast of S. Pietro Island, facing the industrial zone of Taranto, where the S. Nicolicchio rock once stood [35].

The taxonomic nomenclature of the species was updated according to Algaebase (https://www.algaebase.org/, accessed on 2 October 2025).

3. Results

In the Mar Piccolo, based on a comparison of the three floristic lists mentioned above (Table S1), it was found that that, among the species collected by Pierpaoli, 67 species (38 Rhodophyta, 15 Phaeophyceae, and 14 Chlorophyta) and 56 species (32 Rhodophyta, 11 Phaeophyceae, and 13 Chlorophyta) were no longer detected during II and III, respectively. Conversely, 46 species in II (30 Rhodophyta, 3 Phaeophyceae, and 13 Chlorophyta), and 92 species in III (58 Rhodophyta, 13 Phaeophyceae, and 21 Chlorophyta) were not present in Pierpaoli’s lists. Among these, 14 species were NIS, consisting of 9 Rhodophyta, 3 Phaeophyceae, and 2 Chlorophyta (see [24]).

The chorological spectra of the three lists were also analyzed (Figure 3). The biogeographical elements represented include five groups: Atlantic (A), Mediterranean (M), Indo-Pacific (IP), Circumtropical (CT), and Cosmopolite (C) [36]. The percentage of the Cosmopolitan element varied from 38.5% and 40.4% in III and I, respectively. For the Atlantic element, values ranged from 37.2% in III to 42.2% in II. The Indo-Pacific element ranged between 2.2% in II and 5.4% in III, while Circumtropical species accounted 5.6% in II and 7.3% in I. Finally, the Mediterranean element ranged from 11.0% in I to 12.8% in III.

Concerning the Mar Grande basin (Table S2), at S. Nicolicchio rock, a total of 46 species were collected by Pierpaoli in the period 1921–1923, including 15 Rhodophyta, 13 Phaeophyceae, and 18 Chlorophyta. Only 24 of these species were recorded again in 1992, comprising 9 Rhodophyta, 6 Phaeophyceae, and 9 Chlorophyta.

4. Discussion

The benthic algal flora, widely used to monitor coastal ecosystem changes, is considered an effective descriptor of environmental conditions, as it can reflect variations in ecological parameters through its specific richness and community structure, particularly from a long-term perspective [37,38]. In this respect, building a floristic database from historical data is the first step toward understanding changes in biodiversity over time. This information helps us pinpoint the causes of these changes and develop effective conservation and management plans [39].

The availability of historical data from the herbarium MBMP and Pierpaoli’s papers, and of more recent long-term data on the Mar Piccolo monitoring allowed the evaluation of changes occurred over time on phytobenthic communities, as well as their causes. The comparison among the species list relating to the three considered periods highlighted that, over 100 years, the flora underwent noticeable changes. In early 1900s, it was typical of pristine open-sea environments, as indicated by the presence of high-ecological-value canopy-forming species. The disappearance of several sensitive seaweed species—present in the herbarium MBMP but no longer detected in II and III—was evident. These include Cystoseira foeniculacea, Ericaria crinita, E. selaginoides [reported by Pierpaoli as Cystoseira discors (Linnaeus) C. Agardh, C. crinita Duby, and C. erica-marina (S.G. Gmelin) Naccari, respectively] among the Phaeophyceae; Acetabularia acetabulum, Flabellia petiolata (reported as Acetabularia mediterranea J.V. Lamouroux, and Udotea desfontanii Decaisne, respectively), and Halimeda tuna among the Chlorophyta, and Peyssonnelia squamaria among the Rhodophyta. It is worth noting that, regarding Cystoseira spp., only C. compressa and Gongolaria barbata (reported by Pierpaoli as C. abrotanifolia Agardh, and C. barbata Agardh, respectively), both more tolerant species [40,41], have been recorded since. In addition, some shade-adapted species were frequently found at shallower depths than their typical habitat [e.g., Rytiphlaea tinctoria]. Reduced light penetration due to increased sedimentation likely forced deeper-dwelling species to migrate to shallower, more illuminated areas, a phenomenon commonly observed in coastal zones affected by anthropogenic activities [42]

In II, not only were these sensitive species no longer collected, but their epiphytes and understories were also absent. In habitats disturbed by high sedimentation, the loss of canopy species reduces the variety of species between different areas (β-diversity) and increases the number of species that can live in a wide range of conditions (generalist species) [43,44]. Conversely, nitrophilous, sheet-like Chlorophyta (i.e., Ulva spp.) were abundant. Due to their high nutrient uptake efficiency and rapid growth, they reached elevated coverage and biomass [45]; however, their degradation caused severe anoxic crises, as has been reported for other marine areas [46]. Other species tolerant of high nitrogen salt concentrations, such as Gracilaria spp. [47,48], became more abundant and reached high biomass values, forming extensive unattached mats on the increased muddy seabed [34]. Twenty-two sheets of opportunistic species from this period are preserved in the herbarium TAR [30], compared with only six in the herbarium MBMP. In addition, the number of fertile Rhodophyta was somewhat low compared to that inferable from Pierpaoli’s papers and herbarium MBMP. The loss of sexual reproduction is commonly documented as a consequence of anthropogenic disturbances, including eutrophication, heavy metals, and climate change [49]. The most common recovery strategy among seaweeds is the onset of vegetative reproduction [49], as observed in several species in the Mar Piccolo [50]. High sedimentation generally increases vegetative reproduction in resilient seaweeds. These seaweeds can withstand the sediment and tend to regrow from the tough, lower sections of their thalli, more resistant to burial and abrasion. This process, known as fragmentation, is a key strategy for their survival and reproduction in disturbed environments [51]. In the 1920s, the red seaweed Gracilaria dura was observed reproducing via cystocarps in the Mar Piccolo [31]. By the 1990s, however, its reproductive behavior had changed: in autumn, the seaweed’s unattached parts fragmented into modified thallus sections that allowed the species to survive winter and regenerate into new plants the following spring [52]. This shift was undoubtedly a consequence of the high eutrophication of the basin waters, combined increased turbidity, mainly linked to the discharge of untreated effluents into the basin from 14 sewage outlets, both urban and military, since 1920s, and until the late 1990s [53,54,55,56]. Since the early 2000s, most urban sewage outlets have been closed, and the remaining ones have been equipped with treatment plants. Consequently, the chemical and physical conditions of the basin have gradually improved [57]. After sewages closure, among the Phaeophyceae, Colpomenia sinuosa, Padina pavonica, and Sphacelaria cirrosa present in the Pierpaoli’s collection—were again observed colonizing rocks, piers, and quays. Notably, C. sinuosa thrives in nutrient-enriched seawaters [58]; however, low temperature and the presence of natural hard substrata appear to be the main ecological factors limiting its survival [59]. Therefore, the disappearance of most natural substrata and the progressive increase in seawater basin temperature may have contributed to its disappearance. Very few specimens have occasionally been found again in III, so it will be interesting to follow its fate to verify possible adaptations to the new basin environmental conditions. Despite being a very common species, P. pavonica had disappeared from the Mar Piccolo when the environmental conditions worsened significantly. This might be probably due to a low tolerance to the increase in sediment deposit that occurred from the early 1900s onwards. Indeed, several Dictyotales showed this behavior [60,61], and in experiments on subtidal reef patches in the Mediterranean, P. pavonica showed recruitment and survival patterns that depended on the intensity, area, and timing of sand deposition disturbances [62]. The reappearance of this species may confirm a slight improvement in the environmental conditions of the basin [57]. Sphacelaria cirrosa is tolerant to high nitrogen levels in seawater [63]. It is a common epiphyte both on seagrasses and on Cystoseira spp. [64,65,66]. At the same time, it is reported as an epiphyte on some Laminariales and Fucales [67,68]. The disappearance of both seagrasses and Cystoseira spp. from the Mar Piccolo in II, could justify the loss of S. cirrosa from the basin phytobenthic community. Meanwhile, the introduction of two NIS [i.e., Ascophyllum nodosum and Undaria pinnatifida (Phaeophyceae, Laminariales)] [69] and the recovery of a luxuriant Cymodocea nodosa meadow [20], in III, may have fostered the S. cirrosa’s recurrence in the Mar Piccolo and its establishment. Two hypotheses can be formulated for the disappearance of the other sensitive Chlorophyta and Rhodophyta species. Acetabularia acetabulum lives in the upper sublittoral zone in well-illuminated waters [70]; therefore, its disappearance was likely due to both water turbidity and the scarcity of natural hard substrata, which have been gradually replaced by artificial surfaces as human activity increased [60,71]. Flabellia petiolata, Halimeda tuna, and Peyssonnelia squamaria, are sciaphylous species that typically occur from few meters to 60 m in depth, often in association with one another [70]. They were probably understory species of the now-lost Fucales and disappeared together with them.

The chorological spectra plotted for the three periods are consistent with the biogeographic composition of the Italian marine flora, showing a dominance of the Atlantic and Cosmopolitan elements, followed by the Mediterranean one [36]. The variation in both Atlantic and Mediterranean element percentages in III, compared to I, may have been due to the light increase in temperature recorded in the Mar Piccolo in the last twenty-years [72], which limited the settlement and survival of species adapted to lower temperatures [73]. The Cosmopolitan element represents species, which have a wide geographical distribution in the world seas, with a high range of adaptability to the environmental conditions [74]. These species are now defined as eucosmopolitan to distinguish them from the neocosmopolitan species, which have expanded their geographical range as a result of anthropogenic activities (e.g., the introduction of non-indigenous species) [74]. So, the light decrease in the percentage of these species in II compared to I, could be ascribed to the increase in pollution, which caused the disappearance of several Phaeophyceae, many of which belonged to this biogeographic element. The light decrease in III, compared to both I and II, together with the increase in the Circumtropical and Indo-Pacific elements, can be explained by the recent and rapid rise in the number of non-indigenous species (NIS) in the Mar Piccolo, particularly in areas associated with bivalve mollusk importation [24,75]. Solieria filiformis was the first NIS recorded in the Mar Piccolo, in the late 1980s—marking its first occurrence in the entire Mediterranean Sea [76]. The observation of dried specimens uploaded to the herbarium TAR showed a strong resemblance to a specimen stored in the herbarium MBMP, identified as Gracilaria confervoides Greville and collected in the Mar Piccolo in 1922. The observations on the inner anatomical structure of some rehydrated fragments of this last specimen confirmed that they were conspecific [77]. This confirms that herbarium specimens are very useful to ascertain the exact moment in which a NIS appeared in a given area [12]. Moreover, through the molecular analysis of thallus fragments, perhaps it will also be possible to reconstruct the phylogeography of these species [78]. A similar case involves sheet n. 60 of the herbarium MBMP, which preserves a thallus harvested in April 1938 in the port of Ancona and identified as Gracilaria multipartita (Clemente) Harvey. The examination of this specimen during the description of a new species from the bay of Naples, i.e., Gracilaria longa, showed that also the specimen from Ancona belonged to this taxon [79]. This confirms that the discovery and description of new species are often based on examining herbaria. One of the most important phases in the description of a new taxon is the designation of a type specimen, which is a reference sample for the description and classification of a species. This specimen, often kept in an herbarium, is the original specimen referred to when describing and naming a new species. The choice of the sample type is crucial because it serves as a reference for the nomenclature and classification of a plant. When a botanist describes a new species, they must refer to the type of specimen to ensure that its description is accurate and consistent with the original specimen [80].

Concerning the Mar Grande basin, the sensitive Fucales reported by Pierpaoli Ericaria selaginoides (Linnaeus) Molinari & Guiry, Gongolaria barbata f. hoppei (C. Agardh) Falace, Alongi & Kaleb, [as Cystoseira erica-marina (S.G. Gmelin) Naccari, C. hoppei C. Agardh, and C. selaginoides Naccari], and Sargassum hornschuchii C. Agardh, have not been found any more. Similar as observed in the Mar Piccolo, the relatively fast-growing semiperennial C. compressa is still present, which is indicative of anthropized environments with moderately polluted waters since it grows even in harbors [81]. Starting from 1950, Sargassum hornschuchii populations, a species endemic in the Mediterranean, began a progressive and fast reduction up to locally extinction from the southeastern to the northwestern Mediterranean [82]. The main causes of this behavior can be pollution, turbidity, trawling, and seawater temperature increase [82], factors that this zone of the Mar Grande faced in the last 65 years, starting with the establishment of the steel industry. Moreover, this caused over-construction in the coastal area, with a consequent large replacement of natural substrata by concrete, which is known as another cause of biodiversity loss, mainly of canopy-forming species [83].

Herbarium MBMP, storing specimens collected between 1941 and 1946, has proved very useful in detecting changes in seaweed biodiversity also from the Middle Adriatic coasts, particularly along the Conero Riviera. Here, once again, the disappearance of sensitive Fucales, is significant. Among them, Fucus virsoides J. Agardh is of the utmost importance, since it is a glacial relict endemic of the Adriatic Sea. The absence of Peyssonnelia spp. is also worth highlighting [22,26,27]. Moreover, the presence of nine NIS, was observed [22,27].

Herbarium specimens are collected from a vast array of sites and biomes worldide, making them a rich source of data for ecological studies. This diversity allows for the study of functional traits, that is, characteristics of organisms influencing their performance and fitness, going beyond the traditional taxonomic uses of herbaria [84]. For centuries, botanists have collected specimens with reproductive parts (i.e., flowers, fruits), which were essential for species identification. This practice has created vast repositories of phenological data, and the study of phenology has become a major area of research, particularly for higher plants [84]. The same principles of studying phenology from herbarium specimens can be applied to other organisms, such as seaweeds. This is especially important in the context of climate change and human impact, which can alter the life cycles of species [85]. For seaweeds, this can manifest as a loss of sexual reproduction in favor of vegetative reproduction [48]. In this regard, during the study of the seaweed flora of the Gulf of Taranto, propagule-bearing specimens of Alsidium corallinum were observed. Propagules are starch-filled branchlets that serve for vegetative reproduction, as already reported for this species in early descriptions from the Gulf of Naples and other Mediterranean regions [86]. Specimens of Alsidium corallinum with propagules were also collected along the Gargano Promontory (Adriatic Sea). In the herbarium MBMP, two specimens of A. corallinum with propagules (recorded as Hypnea musciformis Lamour), collected in August 1941 along the Conero Riviera, were identified [86]. These findings confirm that propagule formation occurs throughout the Mediterranean and can therefore be considered a species-level trait.

In conclusion, the Pierpaoli herbarium surely has proven to be valuable for research fields on seaweeds across different scientific fields. Its digitization and the sharing of FAIR data [87] will hopefully further enhance its impact. Moreover, the advancements in biodiversity knowledge presented here reaffirm the immense value of Natural Science Collections as indispensable resources for understanding our planet’s biodiversity and history, offering a tangible record of life on Earth.