Introduction
During routine identification of marine zoobenthos collected from Casco Bay, Portland, Maine, a bryozoan new to the Northwest Atlantic was found encrusting shells and barnacles. Zooids presented large areolar pores on their peripheries, lacked pseudopores centrally on their frontal walls, and had a medial avicularium placed just below the primary orifice. These features are among the characteristics of the genus Smittoidea. Worldwide there are 57 species in this genus, 13 of them known from the North Atlantic with only four occurring in the western Atlantic according to the World Register of Marine Species (Ahyong et al., Reference Ahyong, Boyko, Bailly, Bernot, Bieler, Brandão, Daly, De Grave, de Voogd, Gofas, Hernandez, Hughes, Neubauer, Paulay, van der Meij, Boydens, Decock, Dekeyzer, Goharimanesh, Vandepitte, Vanhoorne, Adlard, Agatha, Ahn, Alonso, Alvarez, Amler, Amorim, Anderberg, Andrés-Sánchez, Ang, Antić, Antonietto, Arango, Artois, Atkinson, Auffenberg, Bailly, Baldwin, Bank, Barber, Barrett, Bartsch, Bellan-Santini, Bergh, Berta, Bezerra, Bieler, Blanco, Blasco-Costa, Blazewicz, Błędzki, Bock, Bonifacino, Böttger-Schnack, Bouchet, Boury-Esnault, Bouzan, Boxshall, Bray, Brito Seixas, Broda, Bruce, Bruneau, Budaeva, Bueno-Villegas, Calvo Casas, Cárdenas, Carstens, Cartwright, Cedhagen, Chan, Chan, Choong, Christenhusz, Churchill, Collins, Collins, Collins, Consorti, Copilaș-Ciocianu, Corbari, Cordeiro, Costa, Costa Corgosinho, Coste, Costello, Crandall, Cremonte, Cribb, Cutmore, Dahdouh-Guebas, Daneliya, Dauvin, Davie, De Broyer, de Lima Ferreira, de Mazancourt, de Moura Oliveira, Decker, Defaye, Dekker, Di Capua, Dippenaar, Dohrmann, Dolan, Domning, Downey, Dreyer, Eisendle, Eitel, Eleaume, Enghoff, Epler, Esquete Garrote, Evenhuis, Ewers-Saucedo, Faber, Figueroa, Fišer, Fordyce, Foster, Fransen, Freire, Fujimoto, Furuya, Galbany-Casals, Gale, Galea, Gao, Garic, Garnett, Gaviria-Melo, Gerken, Gibson, Gibson, Gil, Gittenberger, Glasby, Glenner, Glover, Gómez-Noguera, Gondim, Gonzalez, González-Solís, Goodwin, Gostel, Grabowski, Gravili, Grossi, Guerra-García, Guerrero, Guidetti, Guiry, Gutierrez, Hadfield, Hajdu, Halanych, Hallermann, Hayward, Hegna, Heiden, Hendrycks, Hennen, Herbert, Herrera Bachiller, Hodda, Høeg, Hoeksema, Holovachov, Hooge, Hooper, Horton, Houart, Huys, Hyžný, Iniesta, Iseto, Iwataki, Janssen, Jaume, Jazdzewski, Jersabek, Jiménez-Mejías, Jóźwiak, Kabat, Kakui, Kantor, Karanovic, Karapunar, Karthick, Kathirithamby, Katinas, Kilian, Kim, King, Kirk, Klautau, Kociolek, Köhler, Konowalik, Kotov, Kovács, Kremenetskaia, Kristensen, Kroh, Kulikovskiy, Kullander, Kupriyanova, Lamaro, Lambert, Larridon, Lazarus, Le Coze, Le Roux, LeCroy, Leduc, Lefkowitz, Lemaitre, Lichter-Marck, Lim, Lindsay, Liu, Loeuille, Lörz, Ludwig, Lundholm, Macpherson, Mah, Mamos, Manconi, Mapstone, Marek, Markello, Márquez-Corro, Marshall, Marshall, Martin, Martinez Arbizu, McFadden, McInnes, McKenzie, Means, Mees, Mejía-Madrid, Meland, Merrin, Miller, Mills, Moestrup, Mokievsky, Molodtsova, Monniot, Mooi, Morandini, Moreira da Rocha, Morrow, Mortelmans, Müller, Muñoz Gallego, Muñoz Schüler, Musco, Nascimento, Nesom, Neto Silva, Neubert, Neuhaus, Ng, Nguyen, Nielsen, Nielsen, Nishikawa, Norenburg, O'Hara, Opresko, Osawa, Osigus, Ota, Páll-Gergely, Panero, Patterson, Pedram, Pelser, Peña Santiago, Pereira, Pereira, Pereira, Perez-Losada, Petrescu, Pfingstl, Piasecki, Pica, Picton, Pignatti, Pilger, Pinheiro, Pisera, Poatskievick Pierezan, Polhemus, Poore, Potapova, Praxedes, Půža, Read, Reich, Reimer, Reip, Resende Bueno, Reuscher, Reynolds, Richling, Rimet, Ríos, Rius, Rodríguez, Rogers, Roque, Rosenberg, Rützler, Sá, Saavedra, Sabater, Sabbe, Sabroux, Saiz-Salinas, Sala, Samimi-Namin, Santagata, Santos, Santos, Sanz Arnal, Sar, Saucède, Schärer, Schierwater, Schilling, Schmidt-Lebuhn, Schneider, Schönberg, Schrével, Schuchert, Schweitzer, Semple, Senna, Sennikov, Serejo, Shaik, Shamsi, Sharma, Shear, Shenkar, Short, Sicinski, Sidorov, Sierwald, Silva, Silva, Silva, Simmons, Sinniger, Sinou, Sivell, Smit, Smit, Smol, Sørensen, Souza-Filho, Spelda, Sterrer, Steyn, Stoev, Stöhr, Suárez-Morales, Susanna, Suttle, Swalla, Taiti, Tanaka, Tandberg, Tang, Tasker, Taylor, Taylor, Taylor, Tchesunov, Temereva, ten Hove, ter Poorten, Thirouin, Thomas, Thuesen, Thurston, Thuy, Timi, Todaro, Todd, Turon, Uetz, Urbatsch, Uribe-Palomino, Urtubey, Utevsky, Vacelet, Vader, Väinölä, Valls Domedel, Van de Vijver, van Haaren, van Soest, Vanreusel, Velandia, Venekey, Verhoeff, Vinarski, Vonk, Vos, Vouilloud, Walker-Smith, Walter, Watling, Wayland, Wesener, Wetzel, Whipps, White, Wieneke, Williams, Williams, Wilson, Wilson, Witkowski, Wyatt, Xavier, Xu, Zanol, Zeidler, Zhao and Zullini2024). Of these four, three are warm water species, one reported from the Gulf of Mexico (Winston and Maturo, Reference Winston, Maturo, Felder and Camp2009) and two from the Caribbean (Winston and Woollacott, Reference Winston and Woollacott2009; Winston and Jackson, Reference Winston and Jackson2021). The fourth species, Smittoidea propinqua (Smitt, 1868), ranges into the Gulf of Maine from its circumarctic-boreal distribution. The Casco Bay species resembled S. propinqua, but that species does not have a lyrula, the central tooth of a primary orifice which was prominent in the Casco Bay specimens. Using this feature and a suite of other diagnostic characteristics (Osburn, Reference Osburn1952; Soule, Reference Soule1961; Soule and Soule, Reference Soule and Soule1964; Banta, Reference Banta and Brusca1980), the bryozoan was identified as Smittoidea prolifica Osburn, Reference Osburn1952.
Smittoidea prolifica is considered a species of the temperate North Pacific realm (Nelson et al., Reference Nelson, Murray, Otani, Liggan, Kawai, Ruiz, Hansen and Carlton2016) with a fossil record from northern Japan dating from the Neogene (Hayami, Reference Hayami1975). On the western North American coast, this species ranges from Baja California, Mexico to Washington, United States (Figure 1). Osburn (Reference Osburn1952) described S. prolifica from specimens collected from southern California where it was a common shore species that also encrusted floats and pilings. He considered the Smittia reticulata of Robertson (Reference Robertson1908) reported from southern California and the Smittina reticulata of Okada and Mawatari (Reference Okada and Mawatari1936) found in Japan to be S. prolifica. These synonymies established a present-day amphi-North Pacific distribution for this bryozoan which was supported by subsequent records from Japan (Long and Rucker, Reference Long and Rucker1969) and southern Korea (Rho and Seo, Reference Rho and Seo1986; Seo and Min, Reference Seo and Min2009). However, the synonymy of Osburn (Reference Osburn1952) with specimens from Japan and some inconsistencies among species descriptions of specimens collected from southern Korea (Rho and Seo, Reference Rho and Seo1986) have received critical attention (De Blauwe and Faasse, Reference De Blauwe and Faasse2004). In that respect, specimens from the Northwest Pacific require re-examination to confirm their identification so to better understand the North Pacific distribution and morphological variation of S. prolifica.
The global distribution Smittoidea prolifica based on collection locations (closed circles) of specimens used in analyses. Also shown are collection locations for S. spinigera and Parasmittina nitida. Symbology: S. prolifica, green; Smittoidea spinigera, orange; P. nitida, red.
Smittoidea prolifica has a history of introductions in European waters around the North Sea. It was first discovered in 1995 on the southwestern coast of the Netherlands (Van Moorsel, Reference Van Moorsel1996) and at several additional locations there from 1998 to 2001 (De Blauwe and Faasse, Reference De Blauwe and Faasse2004). New records of this species continued to appear along the coastline with discoveries progressing northeastwards (Dekker and Drent, Reference Dekker and Drent2013; Gittenberger et al., Reference Gittenberger, Rensing, Dekker, Niemantsverdriet, Schrieken and Stegenga2015), eventually reaching the Central Wadden Sea coastline of Germany by the German Bight of the North Sea (Markert et al., Reference Markert, Matsuyama, Rohde, Schupp and Wehrmann2015). A few records were reported for offshore locations (Vanagt et al., Reference Vanagt, Van de Moortel and Faasse2013; Kind and Kuhlenkamp, Reference Kind and Kuhlenkamp2016). The most northerly published record of this species was from Tiefe Rinne near Helgoland (Kind and Kuhlenkamp, Reference Kind and Kuhlenkamp2016). Aquaculture and its associated infrastructure were implicated as vectors for introductions (De Blauwe and Faasse, Reference De Blauwe and Faasse2004; Markert et al., Reference Markert, Matsuyama, Rohde, Schupp and Wehrmann2015) as was encrusted floating debris and algae (Markert et al., Reference Markert, Matsuyama, Rohde, Schupp and Wehrmann2015; Kind and Kuhlenkamp, Reference Kind and Kuhlenkamp2016).
In this paper, S. prolifica is redescribed from specimens discovered in Casco Bay, Maine. Morphology is compared, biometrics analysed, and the range of S. prolifica clarified by means of a review of collections from the coasts of the Northeast and Northwest Pacific, the Northwest Atlantic, and locations of introduction in European waters. Finally, preliminary ecological observations are discussed along with possible routes of introduction into the Gulf of Maine.
Materials and methods
Field survey and sample processing
The seabed was sampled near the mouth of the Presumpscot River, Casco Bay, located off Portland (43.6591°N, − 70.2568°W) in Cumberland County on the southern coast of Maine (Figure 2). Quantitative samples, three per station at depths of 4.18 to 7.71 m were taken at four stations approximately 1 h after low tide using a 0.05 m2 Ponar grab sampler. Two stations were sampled on 18 August and the other two on 24 August 2020. Water column environmental parameters were measured with an EXO-1 YSI sonde attached to the grab sampler platform. The platform remained stationary on the bottom for at least 10 min for the sonde to equilibrate before retrieval. Retrieved samples were accessed for general sediment composition and then sifted on deck through a 1 mm mesh sieve. Sorted macrofauna, cobbles, and shells with epibionts were placed in Ziploc® bags containing seawater and stored on ice packs for transport. In the laboratory, all animals were initially sorted to phylum and preserved in 95% ethanol within 24 h of collection. Cobbles and shells were examined by stereomicroscope and preserved whole with attached fauna. Specimens were later identified to the lowest taxon possible, usually species. Voucher specimens of S. prolifica were deposited in the Yale Peabody Museum (YPM), Yale University, New Haven, Connecticut, USA.
Casco Bay, Maine, USA showing location (blue) where Smittoidea prolifica was collected on 18 August 2020 in the Presumpscot River drainage. Other sampling stations (black) yielded no species of bryozoans. Upper inset shows Casco Bay region (frame) and Portland (red) in relation to the Gulf of Maine, New England states, and Canadian provinces.
Imaging
Digital images from light microscopy were taken as tiff files at a resolution of 300 dpi with an Olympus SZ61 stereoscopic microscope system and ImagePro®. Slide scan and SEM images were captured at the Yale Peabody Museum facilities. Slide scan images were acquired using an Olympus BH-51 compound microscope featuring lenses that allow both transmitted (with Differential Interference Contrast filters) and reflected light, outfitted with a Teledyne Lumenera Infinity 3 digital camera. Positioning of the slide, and focus and image acquisition were controlled by software (Objective Imaging Surveyor version 9.4.0.5) along the x, y, and z axes. Individual position images were stitched together on a single plane, and multiple planes rendered into an extended focus image using Helicon Focus Pro version 8.2.0. For SEM, selected specimens were immersed in a sodium hypochlorite solution to remove soft tissue, rinsed in water, air dried, and mounted with double-sided adhesive tape on aluminium SEM stubs. In some cases, specimens were then coated with 6-10 nm gold using a Cressington 208HR high resolution sputter coater. Specimens were observed with a Hitachi SU7000 scanning electron microscope at 15 kV accelerating voltage. All images were stored electronically as tiff files at a resolution of 200 pixels/cm2.
Biometric measurements and analysis
Measurements of mature zooids and zooidal structures were made from tiff files using Adobe Photoshop®. Biometrics were defined according to dimensions illustrated by Pouyet and Herrera (Reference Pouyet and Herrera1986). Measurements were divided among five colonies, each encrusting a separate substrate. Three to eight zooids were measured per colony. Each suite of measurements (zooid length and width, orifice length and width, etc.) was taken from the same zooid. In some cases, structures were obscured or not parallel to the focal plane and could not be reliably measured on a zooid. Because of that, the number of measurements (N) among structures differed. Measurements of specimens from Glen Cove, Vallejo, Solano County, California and Sasebo, Nagasaki Prefecture, Japan were made for comparison with Casco Bay specimens using the same methods with the exception that only one colony was available from these locations. Quadrate shaped zooids were infrequent, present only in the Glen Cove colony, and not measured.
Differences in morphological characters among locations were assessed graphically and statistically. Biometric comparisons of individual characters among locations were performed using one-way Analysis of Variance (SigmaPlot 15) when the data met the assumptions of normality and equal variance according to the Shapiro-Wilks and Brown-Forsythe methods, respectively. When differences among mean values were greater than would be expected by chance, post-hoc multiple comparisons were done using the Holm-Sidak method to find which measures differed statistically from one another. The Kruskal-Wallace test was chosen for analysis when the data did not meet test assumptions. When differences among median values were greater than would be expected by chance, post-hoc multiple comparisons were made using the Dunn's method. Biometric differences in characters between Atlantic and Pacific specimens were assessed by pooling measurements from each ocean and comparing them using a pooled two sample t test when the data met the test assumptions for normality and equal variance, each evaluated the same way as previously described. When test assumptions were not met, the pooled data were compared using the Mann–Whitney test. Finally, specimens were compared to test the hypothesis that zooids had similar average biometrics regardless of the localities they were collected from. Similarity was evaluated using PRIMER 7 nonparametric methods as described by Plymouth Routines in Multivariate Ecological Research (Clarke and Warwick, Reference Clarke and Warwick2001). Initially, the means of each variable (lengths and widths of zooid, orifice, and ovicell) were square root transformed and tabulated for each location. A resemblance matrix was generated from the table using Euclidean distance of the square root transformed means. Finally, dissimilarity among locations was assessed using hierarchal cluster analysis on the resemblance matrix with group average as the cluster mode. Significant differences (P < 0.05) in similarity among locations were evaluated with the similarity profile test (SIMPROF).
Results
Habitat and environmental conditions
The shallow depths (4.18–7.71 m) that specimens of S. prolifica were retrieved from varied little in temperatures (18.98–19.32 °C) and the low salinities (28.86–29.72 psu) were indicative of the Presumpscot River drainage environment (Table 1). Specimens were found in all three grab samples and for each the seabed consisted of unconsolidated sediments with shell. No bryozoans of any species occurred at stations sampled beyond the river where the seabed consisted of primarily soft sediments mixed with sand and gravel.
Geolocation, mean sea bottom environmental attributes, and substrate composition at collection locations of Smittoidea prolifica in Casco Bay, Maine
Colonies encrusted living and dead barnacles (Balanus crenatus Bruguière, 1789) and Mytilus shells with co-occurring Amathia gracilis (Leidy, 1855) and Barentsia laxa Kirkpatrick, 1890. No colonies of S. prolifica were overgrown or overgrew any associated epifauna, and none were found on cobbles. The bryozoan assemblage found on accompanying cobble included dense mats of A. gracilis, along with Cryptosula pallasiana (Moll, 1803) and Pentapora americana (Verrill, 1875).
Systematic account
Order CHEILOSTOMATIDA
Suborder FLUSTRINA
Superfamily SMITTINOIDEA Levinsen, 1909
Family SMITTINIDAE Levinsen, 1909
Genus Smittoidea Osburn, Reference Osburn1952
Smittoidea prolifica Osburn, Reference Osburn1952
(Figures 3–7)
Smittia reticulata Robertson, Reference Robertson1908, p. 306, Plate 23, Figures 75, 76
Smittoidea prolifica Osburn, Reference Osburn1952, pp. 408, 409, Plate 48, Figures 7, 8; Soule, Reference Soule1961, pp. 33, 34; Soule and Soule, Reference Soule and Soule1964, p. 24; Long and Rucker, Reference Long and Rucker1969, p. 63; Banta, Reference Banta and Brusca1980, p. 388, Figure 24.81; De Blauwe and Faasse, Reference De Blauwe and Faasse2004, p. 33, Figures 1, 2; Markert et al., Reference Markert, Matsuyama, Rohde, Schupp and Wehrmann2015, p. 717, Figure 2a–e; Kind and Kuhlenkamp, Reference Kind and Kuhlenkamp2016, p. 1237, Figure 1
Material examined
NORTHWEST ATLANTIC– United States • Maine • Casco Bay, about 100 m north of Martin's Point, Presumpscot River, Cumberland County, Portland: YPM IZ 106905, 43.6910° N, −70.2465° W, depth 6.42 m, Ponar grab, coll. T.J. Trott, 18 Aug 2020, 1 colony on B. crenatus; YPM IZ 106906, 43.6909° N, −70.2968° W, depth 4.18 m, Ponar grab, coll. T.J. Trott, 18 Aug 2020, 1 colony on Mytilus shell; YPM IZ 106907, 43.6909° N, −70.2968° W, depth 4.18 m, Ponar grab, coll. T.J. Trott, 18 Aug 2020, 1 colony on Mytilus shell; YPM IZ 106908, 43.6909° N, −70.2461 W, depth 7.71 m, Ponar grab, coll. T.J. Trott, 18 Aug 2020, 1 colony on Mytilus shell; YPM IZ 106909, 43.6909° N, −70.2968° W, depth 4.18 m, Ponar grab, coll. T.J. Trott, 18 Aug 2020, 1 colony on Mytilus shell; YPM IZ 106910, 43.6909° N, −70.2968° W, depth 4.18 m, Ponar grab, coll. T.J. Trott, 18 Aug 2020, 1 colony on B. crenatus; YPM IZ 106813, 43.6909° N, −70.2461 W, depth 7.71 m, Ponar grab, coll. T.J. Trott, 18 Aug 2020, 1 colony on Balanus plate; YPM IZ 106814, 43.6910° N, −70.2465° W, depth 6.42 m, Ponar grab, coll. T.J. Trott, 18 Aug 2020, 1 colony on Mytilus shell. United States • Virginia • Gates Channel, Accomack County, Wachapreague: USNM 1446003 (SERCINVERT1537), 37° 35.55′ N, −75° 39.51′ W, Trawl-Beam, 1 m, depth 2 m, coll. R. Aguilar, 27 Jun 2017, 1 colony on gravel.
EAST PACIFIC – United States • Washington • Willapa Bay • Boat Basin, Pacific County, Nahcotta: SBNMH 641394, 46° 29.88′ N, −124° 1.98′ W, on old tires, intertidal, coll. K. McCain, 1973, 3 colonies (dry). Oregon • Coos Bay • Empire Boat Ramp, Coos County, Coos Bay: Smithsonian Environmental Research Center (SERC) 30222, 43° 23.5002′ N, −124° 16.8′ W, PVC settlement plate, depth 1 m, coll. E. Collinetti, 2000, 1 colony. Oregon • Coos Bay • Empire Boat Ramp, Coos County, Coos Bay: Smithsonian Environmental Research Center (SERC) 127986, 43° 23.6202′ N, −124° 16.8492′ W, PVC settlement plate, depth 1 m, coll. K. Larson, 2004, 2 colonies. Oregon • South Slough • Crown Point, Coos County, Coos Bay: Smithsonian Environmental Research Center (SERC) 128818, 43° 19.0338′ N, −124° 19.2978′ W, PVC settlement plate, depth 1 m, coll. K. Larson, 2004, 5 colonies. California • Channel Islands • off Santa Cruz Island, Ventura County, Albatross 2945: SBNMH 644249 (voucher), 34° N, −119° 29.502′ W, depth 55 m, coll. unknown, det. R.C. Osburn, 1889, 1 colony (slide). California • Channel Islands • 1 mi SE of Smugglers Cove on Santa Cruz Island, Santa Barbara County, Velero 1295-41: SBNMH 644250 (voucher), 33° 55.75′ N, −119° 31.5′ W, depth 27–38 m, coll. unknown, det. R.C. Osburn, 1941, 1 colony (slide). California • Channel Islands • 1.75 mi SE of Santa Cruz Island, Santa Barbara County, Velero 1662-48: SBNMH 644248 (voucher), 33° 55.75′ N, −119° 31.0833′ W, depth 42 m, coll. unknown, det. R.C. Osburn, 1948, 2 colonies (slide). California • Mission Bay • Dana Marina, San Diego County, San Diego: Smithsonian Environmental Research Center (SERC) 111834, 32° 45.9888′ N, −117° 14.1396′ W, PVC settlement plate, depth 1 m, coll. A.M. Leyman, 2003, 3 colonies. California • San Francisco Bay • Glen Cove Marina, Solano County, Vallejo: Smithsonian Environmental Research Center (SERC) 308827, 38° 24.576′ N, −122° 7.482′ W, PVC settlement plate, depth 1 m, coll. G. Ashton, 2015, 1 colony. California • Humbolt Bay • Eureka Public Marina, Humbolt County, Eureka: Smithsonian Environmental Research Center (SERC) 305986, 40° 48.132′ N, −124° 10.752′ W, PVC settlement plate, depth 1 m, coll. S. Havard, 2015, 1 colony. California • Humbolt Bay • Kuiper Oyster Raft, Humbolt County, North Slough: Smithsonian Environmental Research Center (SERC) 103347, 40° 51.2418′ N, −124° 8.736′ W, PVC settlement plate, depth 1 m, coll. A.M. Leyman, 2015, 3 colonies. Mexico • Baja California • Gulf of California • off Coronado Island, Puritan 145: AMNH 480, 26° 7.142′ N, −111° 16.4455′ W, depth 73–82 m, coll. unknown, det. J.D. Soule, 1957, 1 colony (slide).
NORTHWEST PACIFIC– Japan • Sasebo, Nagasaki Prefecture: USNM 651039, 33° 9.8′ N, 129° 42.7′ E, asbestos/pine wood fouling panel, depth 10 m, coll. Long and Rucker, 1966, 1 colony (dry). Southern Korea • Maldo Island • J.E. Seo private collection, 37° 41.1306′ N, 126° 7.9764′ E, depth 18–23 m, SCUBA, coll. J.E. Seo, 1986.
Description of Casco Bay, Maine specimens
Colony
Unilaminar, glossy, pink, white, encrusting mollusc shells and plates of attached living and dead barnacles. Radiate growth from tatiform ancestrula, young colonies circular but losing shape with progressive development (Figure 3, Figure 4A, B). Largest observed approximately 1.5 cm across.
Smittoidea prolifica from Casco Bay, Maine. Mature colony on Balanus crenatus Bruguière, 1789 with co-occurring Amathia gracilis (Leidy, 1855) and Barentsia laxa Kirkpatrick, 1890. Insets: A, Immature colony on Mytilus shell; B, Close-up of mature colony. Scale: 500 μm. Catalogue numbers: YPM IZ 106813: mature colony; YPM IZ 106814: inset A; YPM IZ 106813: inset B.
Smittoidea prolifica from Casco Bay, Maine. A, Immature colony. Note ancestrula, bottom, middle; B, Same as A in SEM; C, Immature zooid, primary orifice with spines; D, Immature zooids; E, Immature zooid, primary orifice with lyrula and small condyles; F, Mature zooid, primary orifice with spine remnants and prominent condyle. Catalogue numbers: YPM IZ 106814: A to E; YPM IZ 106905: F. Scale: A, B, = 300 μm; C, D = 100 μm; E, F = 50 μm. Scanning electron micrographs by L. Rojas.
Zooids
Zooecia distinct, ellipsoid to irregularly hexagonal, 437–382 μm long ($\bar{x}$
= 414 μm, SD ± 16, n = 22) by 225–382 μm wide ($\bar{x}$
= 267 μm, SD ± 41, n = 22), often separated at lateral and proximal margins by weak ridges formed by adjacent lateral walls.
Frontal wall
Convex, imperforate, smooth in young zooids (Figure 4C, D) becoming rough and more granular in larger zooids (Figure 5). Margin perforated with single row of 10-14 large irregularly sized areolar pores laterally and proximally, often overlapped by ovicells of neighbouring zooids. Ridges between marginal pores weakly developed in young zooids; extend from margin centrally, in later ontogeny becoming so prominent and stout with age to occasionally obscure frontal shield (Figure 5).
Smittoidea prolifica from Casco Bay, Maine. A, Close-up of colony shown in B. Note tubules in lyrulae; B, Slide scan of mature colony, region of close-ups A and C indicated by red rectangle; C, Scanning electron micrograph of same colony. Note small pores outside peristome flaps on the central zooid in C (arrows) and that the peristome does not extend across proximal rim of ovicell. Catalogue number: YPM IZ 106905. Scale: A, 100 μm; B, 500 μm; C, 200 μm. Slide scan by E. Lazo-Wasem. Scanning electron micrograph by L. Rojas.
Orifice
Primary orifice (Figure 4E, F) nearly circular, slightly wider than long, 94–120 μm long ($\bar{x}$
= 109 μm, SD ± 7, n = 22) by 103–132 μm wide ($\bar{x}$
= 120 μm, SD ± 6, n = 22), rounded distally but straighter proximally with prominent medial lyrula. Lyrula, 21–36 μm long ($\bar{x}$
= 27 μm, SD ± 5, n = 21) by 37–56 μm wide ($\bar{x}$
= 47 μm, SD ± 6, n = 21), anvil-shaped (Figure 6A), slightly basally directed with slight longitudinal ridge corresponding with internal tubule (Figure 6B), translucent in light (Figure 5A, Figure 6A). Condyles distinct, subopercular, small in young zooids (Figure 4E) becoming more prominent with age (Figure 4F). Young zooids with four to occasionally five fragile ephemeral hollow spines near distal rim of orifice (Figure 4C), all lost early on except two (Figure 4F) eventually hidden by developing ovicell. Peristome slightly raised in young zooids (Figure 4D, E), later in ontogeny rises proximally appearing flap-shaped on either side of orifice, joining distal surface of umbo and proximal sides of ovicell at its juncture with orifice. Two small extra-aperture small pores, one on each side proximal to primary orifice (Figure 5C).
Lyrula of Smittoidea prolifica from Casco Bay, Maine. A, Light microscope image of a zooid showing internal tube of lyrula; B, Close-up of lyrula with longitudinal ridge corresponding to placement of internal tube; C, Damaged lyrula with distal portion broken off revealing internal tube; D, Sagittally damaged lyrula showing internal tube (arrow). Catalogue numbers: YPM IZ 106905: A to C; YPM IZ 90444: D. Scale: A = 100 μm; B, D = 30 μm; C = 20 μm. Light micrograph by E. Lazo-Wasem. Scanning electron micrographs by L. Rojas.
Avicularia
Single subapertural avicularium, 45–80 μm long ($\bar{x}$
= 60, SD ± 10, n = 18) by 95–112 μm wide ($\bar{x}$
= 104 μm, SD ± 6, n = 18), raised on prominent umbo medial and perpendicular to the frontal wall (Figure 7A, E). Rostrum directed distally. Umbo rounded; spiky with flat distal face in early development (Figure 7B, C), avicularium developing within; avicularium chamber with unadorned pivotal bar; mandible blunt and semicircular (Figure 7D).
Smittoidea prolifica from Casco Bay, Maine. A, Oblique distal view of mature zooids showing avicularia; B, Spiky umbos on developing avicularia of young zooids; C, Spiky umbos on developing avicularia of young zooids, SEM; D, Avicularium of mature zooid with simple unadorned cross bar; E, Lateral view of mature colony showing avicularia projecting upward, perpendicular to the frontal wall. Catalogue number: YPM IZ 106905: A, C, D, E; YPM IZ 106813: B; Scale: A, 150 μm; B, 250 μm; C, 200 μm; D, 20 μm; E, 300 μm. Scanning electron micrographs by L. Rojas.
Ovicell
Prominent, slightly wider than long, 151–216 μm long ($\bar{x}$
= 189 μm, SD ± 18, n = 20) by 214–255 μm wide ($\bar{x}$
= 234 μm, SD ± 12, n = 20), flattened frontally, with scattered pores of varying shape and size, some appearing coalesced forming tube shapes (Figure 5C, Figure 7A). Peristome joins where ovicell corners meet at orifice but does not extend across distal rim (Figure 5C). Granular calcification appears with age as collar enclosing lateral and distal sides of ovicell (Figure 7E). Ovicell rests on distal zooid concealing partially.
Embryo
Orange in life, appearing yellow, white in 90% ethanol.
Polypide
With 12 tentacles.
Remarks
Smittoidea prolifica formed small colonies on mussel shells and attached live and dead barnacles. These specimens bore a close resemblance to those collected from Glen Cove, California and are similar in their general morphology to descriptions from the Northeast Atlantic (De Blauwe and Faasse, Reference De Blauwe and Faasse2004; Markert et al., Reference Markert, Matsuyama, Rohde, Schupp and Wehrmann2015) and East Pacific (Osburn, Reference Osburn1952; Soule, Reference Soule1961; Soule and Soule, Reference Soule and Soule1964; Banta, Reference Banta and Brusca1980). There were subtle differences: occasionally 5 instead of 4 maximum number of ephemeral spines as reported from California (Osburn, Reference Osburn1952; Soule, Reference Soule1961; Soule and Soule, Reference Soule and Soule1964; Banta, Reference Banta and Brusca1980) and the Netherlands (De Blauwe and Faasse, Reference De Blauwe and Faasse2004), no quadrate-shaped zooids as seen in material from California (SERC 305986) and the Netherlands (De Blauwe and Faasse, Reference De Blauwe and Faasse2004), and no twinned ovicells as observed in material from California (SBNMH 644250, SERC 305986) and the Northeast Atlantic (Markert et al., Reference Markert, Matsuyama, Rohde, Schupp and Wehrmann2015; Kind and Kuhlenkamp, Reference Kind and Kuhlenkamp2016). The two small pores proximal to primary orifice have not been described previously but can be seen in Figure 2e of Markert et al. (Reference Markert, Matsuyama, Rohde, Schupp and Wehrmann2015). Zooids were wider than all published measures and the outcomes of an analysis of specimen biometrics follows in the Results. In summary, while these variations are of importance, the general morphology of Casco Bay, Maine specimens did not differ remarkably from previous descriptions.
Regional comparisons of Smittinidae
The only records of Smittinidae in the current study region of the Northwest Atlantic were for S. propinqua (Smitt, 1868), Parasmittina jeffreysi (Norman,1876), and Parasmittina nitida (Verrill, 1875) (OBIS, 2023). Specimens of S. propinqua from the northern Gulf of Maine were examined for comparison (Atlantic Reference Centre: ARC 0057156; ARC 0057157). Smittoidea propinqua resembled S. prolifica primarily by the flap-like shape of the peristome bordering the primary orifice and the presence of a rounded subapertural avicularium. However, S. propinqua was easily distinguished from S. prolifica by the absence of a lyrula.
The similarity of the genus Parasmittina with Smittoidea is superficial since the marginal pores surrounding the frontal wall in Parasmittina are smaller, indistinct, and without ridges between them (Hayward and Ryland, Reference Hayward and Ryland1999). More obvious differences include lateral avicularia with occasional adventitious avicularia instead of a single medial avicularium, ovicells with only a few large perforations instead of scattered pores, and a round rather than oval orifice with either no peristome, e.g., P. jeffreysi, or low and less developed flaps, e.g., P. nitida. Specimens previously identified as S. prolifica from Virginia and deposited at the Smithsonian Institution (USNM 1446003) were examined and determined to be P. nitida.
Towards Establishing the Northwest Pacific Range of Smittoidea prolifica
Remarks
The specimen of S. prolifica collected from a fouling panel from Sasebo, Japan was examined to validate the identification by Long and Rucker (Reference Long and Rucker1969). This single dried specimen, a portion of one of the large colonies found, was similar in general morphology to descriptions from the East Pacific (Osburn, Reference Osburn1952; Soule, Reference Soule1961; Soule and Soule, Reference Soule and Soule1964; Banta, Reference Banta and Brusca1980) and Northeast Atlantic (De Blauwe and Faasse, Reference De Blauwe and Faasse2004; Markert et al., Reference Markert, Matsuyama, Rohde, Schupp and Wehrmann2015) (Figure 8). In particular, each zooid had a single subapertural avicularium oriented perpendicular to the frontal wall, rounded with a pivotal bar without a ligula. Marginal pores separated by ridges surrounded the frontal wall which was not perforated.
Smittoideaprolifica from Sasebo, Japan. A, Whole specimen; B, Colony edge top right, zooid primary orifice distal edge with three remnant spines (arrows). Catalogue number: USNM 651039; Scales: 500 μm. Micrographs by E. Lazo-Wasem.
The specimen collected at Maldo Island, southern Korea (Seo and Min, Reference Seo and Min2009) was re-examined from an unpublished SEM sent to the author by J.E. Seo (Figure 9). Using Liu et al. (Reference Liu, Yin and Ma2001) as a guide, the specimen was determined to be Smittoidea spinigera (Liu, Reference Liu1990). The specimen was re-examined by J.E. Seo and agreement was met with the revised identification. Diagnostic characters were the orientation of the suboral avicularium that was directed obliquely upward and the presence of a ligula on the pivotal bar. In S. prolifica, the suboral avicularium was oriented perpendicular to the frontal plate (Figure 7E) and the ligula was lacking (Figure 7D). Also noteworthy were the relatively large marginal pores that sometimes occupied most of the frontal plate, a situation resembling species of the genus Smittina (Figure 2A-D in Liu, Reference Liu1990).
Smittoideaspinigera (Liu, Reference Liu1990) from Maldo Island, southern Korea. Note the obliquely upward directed orientation of the suboral avicularia and ligulas on pivotal bars. Relatively large marginal pores occupy most of the frontal plate on some zooids. Scale: 500 μm. Scanning electron micrograph by Ji Eun Seo. (Courtesy of Ji Eun Seo).
Reconsideration of the Northwest Pacific range
De Blauwe and Faasse (Reference De Blauwe and Faasse2004) raised questions concerning potential differences in the morphology of the specimens collected from the Northwest Pacific and called for re-examination. The current study confirmed the identification of Long and Rucker (Reference Long and Rucker1969) of S. prolifica in Japan. On the other hand, specimens of Seo and Min (Reference Seo and Min2009) from southern Korea were S. spinigera. Another Northwest Pacific record questioned by De Blauwe and Faasse (Reference De Blauwe and Faasse2004) concerned the specimen collected in southern Korea and described as S. prolifica by Rho and Seo (Reference Rho and Seo1986). Specifically, potential differences involved the size and distribution of pores on ovicells, number and shape of spines, and protracted orifice. These features were re-examined by J.E. Seo and the present author. The raised margins on the ovicell pores seen in the light micrograph Plate 11, Figure 1 of Rho and Seo (Reference Rho and Seo1986) aligned this specimen with S. spinigera, not S. prolifica, as did the obliquely upward orientation of the suboral avicularium and a ligula on the pivotal bar, though this was infrequent. The number of ephemeral spines was three, but re-examination showed that number was based on the spines that remain during ovicell development as shown in the current paper for S. prolifica (Figure 4F). Examination of zooids of S. spinigera from Maldo Island in zones of astogenic growth found they had 4-7 spines, and the ancestrula had 9 spines. In summary, all records of S. prolifica in southern Korea were mistaken identifications of S. spinigera and the localities of occurrences there were therefore unsupported.
The occurrence of S. prolifica in Japan reported by Rho and Seo (Reference Rho and Seo1986) was based on the opinion of Osburn (Reference Osburn1952) who equated the S. reticulata of Okada and Mawatari (Reference Okada and Mawatari1936) from Japan with S. prolifica. The grounds for Osburn's judgement were found to be vague and unpersuasive by De Blauwe and Faasse (Reference De Blauwe and Faasse2004) because mandible shape and orientation were not considered, only the placement and shape of the avicularium. In particular, the mandible of S. prolifica was rounded, not acute as described by Okada and Mawatari (Reference Okada and Mawatari1936) who also stated it ‘pointed downward,’ which could mean directed proximally or perpendicular to the frontal plane as in S. prolifica. This ambiguity in meaning was clarified in the present study by reviewing the specimen from Sasebo, Japan as well as other species descriptions in Okada and Mawatari (Reference Okada and Mawatari1936) that were accompanied by text figures. When ‘pointed downward(s)’ was used, mandibles were directed proximally. Examples of this were given in the descriptions of Pleurocodonellina signata (Waters, 1889), i.e., Smittina elongata Okada and Mawatari, Reference Okada and Mawatari1936 and Parasmittina rouvillei (Calvet, 1902). Also included in this group was their new species Smittina projecta, an obvious Parasmittina, and is revised here to Parasmittina projecta (Okada and Mawatari, Reference Okada and Mawatari1936). Clearly, given this clarification, the S. reticulata of Okada and Mawatari (Reference Okada and Mawatari1936) was not S. prolifica and consequently locations for S. prolifica in Japan stemming from Osburn (Reference Osburn1952) are unsound. In summary, the only valid records of extant S. prolifica in the Northwest Pacific are those of Long and Rucker (Reference Long and Rucker1969) from Sasebo, Japan.
Biometric comparisons among geographically widely separated locations
Measurements of zooid characters from Maine colonies varied in comparison to sizes from other locations with statistical significance, but only one character, zooid width, proved largest among all recorded for that biometric (Table 2, Figures 10 and 11). Otherwise, when biometric differences occurred among locations, none were unique to Maine. For example, Maine and Japan zooid lengths were significantly different and smaller than measures from California and Germany specimens (Figure 11). Primary orifice length was significantly different and smaller for Maine and Japan compared to California, however it was smallest for Germany as was orifice width that was significantly different from all locations. Ovicell length was significantly different and smaller for Maine, Germany, and Japan compared to California, but among all locations it was significantly different and smallest for Germany. Ovicell width was significantly different and smallest for Germany followed by Japan, each significantly different and smaller than California and Maine. In summary, California zooids were larger in all dimensions except zooid width and Germany the smallest except for zooid length. No location was significantly dissimilar when averages of all biometrics per locality were compared (P = 0.12, SIMPROF test; Figure 12). However, specimens from Germany were most different with hierarchal cluster analysis placing them on a separate branch (Figure 12). Comparisons of biometrics between oceans showed that Pacific and Atlantic specimens differed significantly in all measures except zooid length and orifice width (Figure 13). Zooid width was the only character that was significantly different (U = 453, P = 0.043) and larger for Atlantic specimens compared to Pacific ones.
Measurements of Smittoidea prolifica collected from the Northwest Atlantic (Maine), East Pacific (California), Northwest Pacific (Japan), and the Northeast Atlantic (Germany)
Measurements of Smittoidea prolifica from widely separated geographic locations arranged from NE Atlantic to NW Pacific. A, Zooid length; B, Zooid width; C, Orifice length; D, Orifice width; E, Ovicell length; F, Ovicell width. Abbreviations: CA, California; GR, Germany; JP, Japan; ME, Maine. Symbology: Mean, solid black circle; Standard deviation, box; Maximum and minimum values, whiskers (visible only when exceeding SD). Data used to construct plots are presented in Table 2.
Contrasts of character measurements of Smittoidea prolifica from geographically widely separated locations. Matrices are interpreted by comparing column with row labels. Coloured squares indicate statistical significance: light pink, P < 0.05; pink, P < 0.01; red, P < 0.001). Numbers are mean measurements (μm). Abbreviations: CA, California; GR, Germany; JP, Japan; ME, Maine.
Dendrogram of zooid biometrics of colonies of Smittoidea prolifica collected from geographically widely separated locations, using group-average clustering from Euclidean similarities on square root transformed averages. No locations differed significantly as indicated by the red dotted lines (P = 0.12, SIMPROF test). Abbreviations: CA, California; GR, Germany; JP, Japan; ME, Maine.
Statistical comparisons of biometrics of zooid characters pooled among Atlantic (Germany and Maine) and Pacific (California and Japan) specimens of Smittoidea prolifica. Red indicates which ocean had the larger measurement when test results were statistically significant (P < 0.05).
Discussion
The discovery of S. prolifica in Casco Bay, Maine, is the first for the Northwest Atlantic Ocean. There are no reports of Smittinidae in Casco Bay dating back to the earliest and exhaustive 1873 faunal surveys by Verrill (Reference Verrill1874a, Reference Verrill1874b), so it is unlikely that S. prolifica was present there prior to this finding and misidentified. On a broader geographic scale, the only records of Smittinidae in the Gulf of Maine are for P. jeffreysi, P. nitida, and S. propinqua. The chance of confusing the identities of these species with S. prolifica is small. So, while misidentification of an introduced species as a local species does occur (Chapman, Reference Chapman1988), the obvious distinguishing features of these co-occurring species make that error improbable. The chance for misidentification is reduced further by other more detailed characteristics which differentiate these species.
Specimens of S. prolifica from Casco Bay, Maine were morphologically indistinguishable from ones collected at geographically widely dispersed locations in the temperate North Pacific and places of introduction in northern European waters. However, comparisons among locations revealed that a few characteristics varied. The number of ephemeral spines was up to five in Maine specimens, 2 or 3 in Germany (Markert et al., Reference Markert, Matsuyama, Rohde, Schupp and Wehrmann2015), and 2 to 4 in southern California (Robertson, Reference Robertson1908; Osburn, Reference Osburn1952), Baja California (Soule and Soule, Reference Soule and Soule1964), Gulf of California (Soule, Reference Soule1961; Banta, Reference Banta and Brusca1980), and the Netherlands (De Blauwe and Faasse, Reference De Blauwe and Faasse2004). The number of marginal pores, 10 to 14 for Maine specimens, agreed with a ‘dozen or so’ reported by Banta (Reference Banta and Brusca1980) but was less than 18 to 22 and 16 to 18 described by Soule (Reference Soule1961) and Soule and Soule (Reference Soule and Soule1964), respectively. Zooecia shape was most frequently described as ovate and ellipsoid to irregularly hexagonal like for Maine specimens but was also quadrate for the Netherlands (De Blauwe and Faasse, Reference De Blauwe and Faasse2004) and some specimens from California (personal observation). There were no instances of zooids with twin ovicells seen in specimens from Germany (Markert et al., Reference Markert, Matsuyama, Rohde, Schupp and Wehrmann2015; Kind and Kuhlenkamp, Reference Kind and Kuhlenkamp2016) and California (personal observation). In summary, some morphological characteristics of S. prolifica were variable and whether this is of minor in consequence or carries some significance is subject to further study.
Some features of Maine specimens were not included in previous descriptions of S. prolifica. For zooids in zones of astogenic growth, the umbo was spiky with a flat distal face in early development and not rounded as it appeared later in development. There were two small extra-aperture pores, one on each side of primary orifice, proximally. Also, the lyrula had a longitudinal ridge that corresponded with a medial translucent tubule visible in light microphotographs that was drawn in Figure 8 by Osburn (Reference Osburn1952) but not described. The tubule was internal to the lyrula and no connection to the avicularium chamber was seen.
Specimens of S. prolifica from different locations were remarkably similar in morphometry, none being statistically dissimilar in comparisons of their averaged zooid biometrics. If significant dissimilarity had been found, that could have raised questions about conspecificity. When individual character measurements were compared, however, there were significant variations. In general, biometrics of California specimens were the largest and Germany the smallest, a trend in difference that continued on a broader spatial scale when biometrics were compared by ocean. Maine specimens did not stand out as being particularly different biometrically and varied most by one character alone, zooid width, that was the largest among its measurements from all localities. For the remaining biometric comparisons, there was always one other location in common with Maine that had significantly different measures. A statistical evaluation unfortunately could not be done using all published character measurements. Only ranges in zooid length and width were published for specimens from the Netherlands and the number of measurements that determined the ranges were not (De Blauwe and Faasse, Reference De Blauwe and Faasse2004). The raw data were not available to be assessed for normality and equal variances, and ranking. That said, the range in ovicell width (200–250 μm) was greatest among measurements for specimens from the Netherlands, as was zooid length (500–700 μm) (De Blauwe and Faasse, Reference De Blauwe and Faasse2004). These biometrics blur conclusions about larger biometrics for S. prolifica in its native vs introduced range that might otherwise be made. As for differences in biometrics, some of the character variation among locations might be explained by differences in sea water temperature since its effects on bryozoan growth and zooid morphology are known (O'Dea and Okamura, Reference O'Dea and Okamura1999; Amui-Vedel et al., Reference Amui-Vedel, Hayward and Porter2007; Okamura et al., Reference Okamura, O'Dea and Knowles2011). Likewise, such differences could be the consequence of genotypic variation (Hageman et al., Reference Hageman, Bayer and Todd1999).
In its native range and locations of introduction, S. prolifica occurred in subtidal and intertidal habitats, within a broad range of temperatures and salinities, and on a diversity of substrates. Water temperatures ranged from 8.6 °C (Long and Rucker, Reference Long and Rucker1969) to tropical waters (Soule and Soule, Reference Soule and Soule1964) with salinities spanning brackish (De Blauwe and Faasse, Reference De Blauwe and Faasse2004) to full sea water. Features of the subtidal habitat where Maine specimens occurred were within the limits of these environmental conditions. Substantially more is known about the kinds of substrates S. prolifica attaches to where it was introduced than in its native range where only general information was published with species descriptions (Robertson, Reference Robertson1908; Osburn, Reference Osburn1952; Soule, Reference Soule1961; Soule and Soule, Reference Soule and Soule1964; Banta, Reference Banta and Brusca1980). Biogenic (empty shells or shells of living animals, wood, macroalgae), inorganic (rocks ranging in size from small stones to boulders), and artificial (floats and fouling panels made of asbestos/wood or PVC) substrates were colonized. In Maine, S. prolifica encrusted mussel shells and plates of attached living and dead barnacles as reported elsewhere (e.g., Markert et al., Reference Markert, Matsuyama, Rohde, Schupp and Wehrmann2015). The low specificity for attachment substrates was contrary to not finding S. prolifica on seawalls around Helgoland (Kind and Kuhlenkamp, Reference Kind and Kuhlenkamp2016), an observation which might imply that wave exposure influenced successful colonization. In summary, S. prolifica is a eurythermal and euryhaline species with low substrate specificity. These features indicate a high potential for successful introduction into subtidal habitats and wave protected bays and harbours.
The source populations where Casco Bay S. prolifica originated were most likely in the Northeast Atlantic at locations of established introductions in the North Sea. Portland is the only container cargo port in Maine, a major New England seaport (Anonymous, 2001; United States Department of Transportation, 2018) that is currently experiencing record growth in imports (LaClaire, Reference LaClaire2022). This port receives commerce with container ships originating in the North Sea (McGuire, Reference McGuire2019) and likely the biofouling communities which can establish on such vessels (Davidson et al., Reference Davidson, Brown, Systma and Ruiz2009). Ship-borne species spread is unquestionable at global scales (Carlton, Reference Carlton1996; Seebens et al., Reference Seebens, Gastner and Blasius2013; Cuthbert et al., Reference Cuthbert, Kotronaki, Carlton, Ruiz, Fofonoff and Briski2022) and is understood at finer scales among ports using eDNA metabarcoding (Andrés et al., Reference Andrés, Czechowski, Grey, Saebi, Andres, Brown, Chawla, Corbett, Brys, Cassey and Correa2023). Knowing the haplotype network for native and introduced populations would be valuable for understanding the dispersal of S. prolifica into the Northwest Atlantic and elsewhere. More extensive taxonomic and morphological comparisons could reveal patterns in phenotypic character variation to complement and aid the interpretation of genetic analyses like was done by Dick et al. (Reference Dick, Waeschenbach, Trott, Onishi, Beveridge, Bishop, Ito and Ostrovsky2020) for the bryozoan Juxtacribrilina mutabilis (Ito, Onishi & Dick, 2015).
The issue of the timing for the arrival of S. prolifica into Casco Bay can be explored through a brief history of Portland's commercial shipping industry as it relates to ship-borne species spread. In 1999, over 90% of ballast water discharge into Casco Bay did not undergo any at sea exchange (Ruiz et al., Reference Ruiz, Miller, Lion, Steves, Arnwine, Collinetti and Wells2001), a process voluntary at a time when Portland was the second largest oil port on the US East coast (Anonymous, 2001). Portland kept that shipping status until 2016. The origin of oil shipments was not overseas. Portland container cargo commerce with North Sea seaports began in earnest in 2013 (Bennett, Reference Bennett2016). In 2018, two introduced species, the bryozoan Juxtacribrilina mutabilis and the amphipod Grandidierella japonica Stephensen, 1938, were discovered in Casco Bay during benthic surveys. The North Sea was likely the ultimate source of these introductions into the Northwest Atlantic (Trott and Enterline, Reference Trott and Enterline2019; Dick et al., Reference Dick, Waeschenbach, Trott, Onishi, Beveridge, Bishop, Ito and Ostrovsky2020; Trott et al., Reference Trott, Lazo-Wasem and Enterline2020). The following year an eelgrass (Zostera marina Linnaeus, 1753) faunal survey (Maine Coastal Program, 2019) tracked the occurrence of J. mutabilis and G. japonica during summer-fall but did not sample the location where S. prolifica was found by the present study. This contemporary bay-wide benthic investigation was only the second one ever conducted, the first in 1980 that did not find these invasives (Larsen et al., Reference Larsen, Johnson and Doggett1983). Considering the timing of discoveries, probable source populations, and the history of Portland container cargo commerce, S. prolifica was most likely introduced in 2013 or thereafter. None of the three introductions were found by ongoing regional invasive monitoring programmes that primarily monitor floating docks. These are the Rapid Assessment Survey (RAS) and Marine Invader Monitoring and Information Collaborative (MIMIC) established in 2000 (Pederson et al., Reference Pederson, Bullock, Calder, Carlton, Chapman, Cohen, Dean, Drynda, Harris, Lambert, Lambert, Mathieson, Tyler, Winston and Barrett-O'Leary2001) and 2006 (Massachusetts Office of Coastal Zone Management, 2024), respectively. The unquestionable success of these programmes has been proven through their discoveries of species introductions and tracking range shifters. Adding a benthic survey component to their protocols would diversify the types of habitats examined and consequently improve their power of detection.
Establishment of S. prolifica beyond the scope of Casco Bay seems likely if its history of invasion in northern Europe is an indication of its success. This species has low substrate specificity and broad tolerance of environmental conditions. In fact, the success of this species being introduced and established makes it difficult to rule out the possibility that it was introduced into Sasebo, Japan by ships originating in California. The impact of S. prolifica may be low as predicted in the Netherlands (De Blauwe and Faasse, Reference De Blauwe and Faasse2004). However, while invasive species with negligible effects often provoke slight to no concern, that dismissive perspective belies the significance of their signal of species arriving outside of their native range. Indifference risks playing ecological roulette in a time of unprecedented unpredictability, and the detection of three invasives in the course of three years in Casco Bay, each of them new to the Northwest Atlantic, gives a strong signal of more introductions to come.
Data
The data that support the findings of this study are available from the corresponding author upon reasonable request.
Acknowledgements
I express my sincere appreciation and gratitude to the many who helped during the development of this project in various indispensable ways. The helpful and constructive readings with discussion by Hans De Blauwe, external collaborator at Royal Belgian Institute of Natural Sciences, Eric Lazo-Wasem, Division of Invertebrate Zoology, Peabody Museum, Yale University, Linda McCann, Smithsonian Environmental Research Center (SERC), and Ji Eun Seo, Department of Life Science, Woosuk University lead to a much-improved manuscript. Lily Berniker, Division of Invertebrate Zoology, American Museum of Natural History, Vanessa Delnavaz, Division of Invertebrate Zoology, Santa Barbara Museum of Natural History, William Moser, Department of Invertebrate Zoology, National Museum of Natural History, and Nicholas Drew and Jessica Nakano, Department of Paleobiology, National Museum of Natural History prepared and sent loans of specimens. Linda McCann and Natasha Hitchcock of the Smithsonian Environmental Research Center sent additional specimens. Ji Eun Seo of the Woosuk University Department of Life Science supplied SEM images of specimens from southern Korea and kindly joined in helpful and essential discussions on identifications. The efforts of all the SERC staff, interns, and fellows who tirelessly processed fouling panels and vouchered specimens are gratefully acknowledged. A special thank you to Claire Goodwin, Huntsman Marine Science Centre, New Brunswick, Canada for providing access to specimens from the Atlantic Reference Centre. Alexandra Markert and Kei Matsuyama generously shared their biometric data from specimens collected in Germany. Eric Lazo-Wasem and Lourdes Rojas of the Peabody Museum of Natural History, Yale University, provided expert technical support and light and SEM imagery. Fieldwork was supported by the Maine Department of Environmental Protection and the Maine Coastal Program. My heartfelt appreciation to the crew of the R/V Amy Gale for assistance in the field. I thank the anonymous reviewer and Paul D. Taylor, Natural History Museum, London for constructive comments which greatly improved the quality of the manuscript.
Financial support
This research received no specific grant from any funding agency, commercial or not-for-profit sectors.
Competing interests
Not applicable.
Ethical standards
Not applicable.
