Mechanisms of habitat segregation between an invasive (Mytilus galloprovincialis) and an indigenous (Perna perna) mussel: adult growth and mortality

The invasive mussel Mytilus galloprovincialis and the indigenous mussel Perna perna coexist intertidally on the south coast of South Africa through partial vertical habitat segregation: M. galloprovincialis dominates the upper shore and P. perna the lower shore. Recruitment patterns can explain the zonation of P. perna, but not the invasive species. We examined the role of post-recruitment interactions by measuring spatial and temporal differences in adult growth and mortality rates of the two species. Specifically, we tested the hypothesis that interspecific differences in growth and mortality reflect adult distribution patterns. The two study locations, Plettenberg Bay and Tsitsikamma, are 70 km apart with two sites (separated by 300–400 m) per location, each divided into three vertical zones. Growth was measured seasonally using different marking methods in 2001 and 2003. Cumulative adult mortality was measured through summer in 2003/2004. Both species generally grew more slowly upshore, but they showed different effects of season. For P. perna, growth was significantly reduced in winter in the low zone, but unaffected by season in the high zone. For M. galloprovincialis, growth was either unaffected by season or increased in winter, even in the high zone. Thus, growth of P. perna and M. galloprovincialis was reduced under cool winter and warm summer temperatures, respectively; and while growth was more similar between species in summer, M. galloprovincialis grew much faster than P. perna in winter. Mortality of P. perna increased upshore. For M. galloprovincialis, mortality was not zone-dependent and was significantly greater than for P. perna on the low-shore and (generally) across the shore in Tsitsikamma. Both species had higher growth and mortality rates in Plettenberg Bay than in Tsitsikamma. Thus, P. perna seems able to maintain spatial dominance on the low-shore and at certain sites because of higher mortality of M. galloprovincialis. We conclude that seasonality in growth of the two species reflects their biogeographic affinities and that coexistence is possible through pre-recruitment effects that limit the vertical distribution of P. perna and post-recruitment effects that limit M. galloprovincialis

Will the invasive mussel Mytilus galloprovincialis Lamarck replace the indigenous Perna perna L. on the south coast of South Africa?

The mussel Mytilus galloprovincialis is invasive worldwide, has displaced indigenous species on the west coast of South Africa and now threatens Perna perna on the south coast. We tested the hypothesis that Mytilus will replace Perna by examining changes in their distribution on shores where they co-exist. Total cover, adult density, recruit density, recruit/adult correlations and mean maximum lengths of both species were measured in 2001 at two contrasting sites (Plettenberg Bay and Tsitsikamma) 70 km apart, each including two locations 100 m apart. Cover and density were measured again in 2004. Total mussel abundance was significantly lower in Tsitsikamma, and recruit density was only 17% that of Plettenberg Bay. Abundance and cover increased upshore for Mytilus, but decreased for Perna, giving Mytilus higher adult and recruit density and total cover than Perna in the upper zones. Low shore densities of recruits and adults were similar between species but cover was lower for Mytilus, reflecting its smaller size, and presumably slower growth or higher mortality there. Thus, mechanisms excluding species differed among zones. Recruitment limitation delays invasion at Tsitsikamma and excludes Perna from the high shore, while Mytilus is excluded from the low shore by post-recruitment effects. Recruitment limitation also shapes population structure. Recruit/adult correlations were significant only where adult densities were low, and this effect was species-specific. Thus, at low densities, larvae settle or survive better near adult conspecifics. After 3 years, these patterns remained strongly evident, suggesting Mytilus will not eliminate Perna and that co-existence is possible through partial habitat segregation driven by recruitment limitation of Perna on the high shore and post-settlement effects on Mytilus on the low shore

Pseudostomella mandela Todaro, Perissinotto & Bownes, 2015, n. sp.

Pseudostomella mandela n. sp. Figs. 6–9 ZooBank lsid:zoobank.org:act:C 8 FA 4 EBD- 5939 - 4 F 79 -AD 7 F- 4 CB02FE 184 CA Type locality. South Africa, KwaZulu-Natal, Cape Vidal, iSimangaliso Wetland Park (Latitude 28 °07’ 18 ” S; Longitude 32 ° 33 ’ 43 ” W); at about 1.5 m water depth, in fine to medium, well sorted sand (mean grain size, 0.246 mm; sorting, 0.46). Values of salinity and pH of coastal waters around the time of sampling were 36.8 and 8.4, respectively, with temperatures ranging from 27–28 ° C. Other locations. Umhlanga (Durban) at 5 m water depth in fine, moderately well sorted siliceous sands (mean grain size, 0.228 mm sorting, 0.51); St. Lucia beach, at mid-tide level in medium-sized, moderately sorted, siliceous grains on a high-energy sandy beach (see Todaro et al. 2011 b). Type specimens. Holotype: the 477 Μm long adult specimen shown in Figure 7, no longer extant (International Code of Zoological Nomenclature, Articles 73.1. 1 and 73.1.4), collected on 2 February 2013 (MAT legit). Additional material examined. Five adult specimens, four collected by the author from the type locality and one from Umhlanga, all were observed alive and are no longer extant. Three further identified specimens were fixed in alcohol and are kept in the collection of the first author. Ecology. Frequency of occurrence: common in sediment along the ocean shore of the iSimangaliso Wetland Park, usual in southern sites near Durban. Abundance: prevalent to numerous in sub-littoral sediment at 1.5 m, scarce in deeper and littoral sediments where found. Diagnosis. A Pseudostomella with an adult TL up to 481 µm; pharynx length up to 105 µm, with pharyngeal pores at base. PhIJ at U 33; body slender, with fine lines and elongate, furcate caudum. Head with mid-sized fleshy preoral palps curving forward; palps showing few sensory hairs and provided with 5 and 6 papillae on the dorsal and ventral border respectively. Sensory hairs sparse but evenly spaced on the body, forming two columns from about U 11 to U 89; epidermal glands barely visible, asymmetrically scattered along most of the length of the body. Cuticular armature of medium-size tetrancres on whole dorsal and ventrolateral surface. Adhesive tubes: TbA, 4 per side, a small one medially and 3 larger ones laterally, forming an arc; TbDL, 1 per side, inserting on lateral margin of the posterior trunk region at U 90; TbVL, 11 per side, of considerably variable length, irregularly spaced along the intestinal region from U 40 to U 81; the last two tubes appearing very close to each other but not sharing a common base; TbP, 4 per side, 2 + 1 at the end of each caudal pedicle the other one flanking each pedicle medially; cirrata tubes, 7 per side, 2 smaller ones inserting laterally along the pharyngeal region at U 16 and U 32 respectively, and 5 larger ones inserting dorso-laterally on the trunk from U 48 to U 87; the last one particularly large. Ventral locomotory cilia: a continuous field of transverse rows covering sparsely the entire ventral surface except the anogenital area. Reproductive system: testis on the right body side, sperm duct noticeably swollen at the confluence of the ano-genital area; caudal organ inverted, pyriform, at U 80; frontal organ, small, bladder-like, at U 77; maturing eggs mid-dorsally above the intestine. Etymology. The species is dedicated to the late Nelson Rolihlahla Mandela, the first democratically elected President of South Africa and 1993 Nobel Peace Prize awardee. Description. The description is mainly based on the adult holotype specimen, 477 µm in total length, shown in Figure 6. Body somewhat slender, a little swollen in the posterior pharyngeal region and at the base of the 44 µm long caudal pedicles. Pharynx 104 µm in length, measured from the ventral border of the oral opening to the pharyngeo-intestinal junction; pharyngeal pores near the base at U 31; pharyngeo-intestinal junction at U 33; widths of neck\PhIJ\trunk\caudal base are 45 \ 41 \ 57 \ 28 µm at U 22 \U 33 \U 51 \U 91, respectively. Head with well developed, fleshy preoral palps, curving ventromedially; the dorsal border projecting just beyond the ventral. Sensory hairs and papillae present on dorsal and ventral borders of the preoral palps; hairs are scattered on the dorsal, lateral and ventral surface of the palps; dorsally there are five papillae, nearly of the same length (5–7 µm), symmetrically arranged along the inner border of the palps in a 2 + 1 + 2 pattern; ventrally, there are six clearly recognizable papillae, 3–6 µm in length, symmetrically arranged more centrally about the inner border of the palps in a 3 + 3 pattern; all papillae bearing one or two short sensory hairs at their tip; other sensory cilia form lateral columns that are more or less evenly spaced from U 11 to U 89; individual hairs are 12–15 µm in length. A variable number of additional papillae, much smaller in size (1–3 µm), can be found ventrally along the inner border of the palps. Epidermal glands barely visible, variable in shape (oval to oblong) and size (5–8 µm in diameter), asymmetrically scattered along most of the length of the body. Cuticular armature. Mid-sized tetrancres with delicate, nearly straight lines, taller than wide (3 x 2 µm – 10 x 7 µm) on the whole dorsal and ventrolateral surface; posteriorly ancres do not extend onto the caudum. Adhesive tubes. TbA, 4 per side, a small one medially (3 µm in length) and 3 larger ones laterally (7–8 µm in length), forming an arc at U09-U 10; TbDL, 1 per side (14–16 µm in length), inserting on the lateral margin of the posterior trunk region at U 90; TbVL, 11 per side, of different size, irregularly spaced along the intestinal region from U 40 to U 81; 5 tubes are visibly larger (23–29 µm in length) and 6 are smaller (11–17 µm in length) than the others; the last two smaller tubes appear very close to each other yet they seem to originate independently, i.e. do not share a common base; TbP, 4 per side, 2 + 1 (5–6 µm in length) at the end of each pedicle of the furcated caudum and the other one (10–11 µm in length) flanking each pedicle medially. Ventral locomotory cilia. A continuous field of transverse rows covering sparsely the entire surface except around the ano-genital area at U 85. Reproductive system. Testis on the right body side, sperm duct noticeably swollen at the confluence of the anogenital area; caudal organ inverted, pyriform (35 µm long x 15 µm wide), at U 80; frontal organ, bladder-like (10–12 µm in diameter) at U 77; maturing eggs mid-dorsally above the intestine. Variability and remarks. The body length of 6 living specimens ranged from 465 to 481 µm (mean = 476.6 µm SD = 5.3 µm), all of them were mature (i.e. showed at least the testis filled with sperm). One specimen (TL = 480 µm) showed an asymmetry in the TbA by virtue of a supernumerary fifth tube on the right side (Fig. 9); the adhesive tubes of the TbVL series showed some variability in number, depending on individuals, ranging from 10 to 13 tubes; however, in all specimens the last two tubes were very close to each other with the longest of the two being the terminal one. Although the last two tubes appear to originate independently under DIC optics, a final word on this matter would necessitate a SEM survey. In a previous study, we reported on a juvenile specimen of Pseudostomella found at St Lucia beach (iSimangaliso Wetland Park, Todaro et al. 2011 b). The cuticular covering, made up of tetrancres, the rather long caudal pedicles and the same area of the finding leave no doubt that the current adult specimens and the juvenile found previously belong to the same species. This is despite some differences regarding the presence of TbL in the juvenile but not in the adults, which bear cirrata tubes instead. Cirrata tubes have been described for several thaumastodermatid species e.g., Tetranchyroderma (Todaro 2002) and are generally thought to convey the secretions (probably with a repellent function) produced by the epidermal glands externally. The densely packet droplets clearly visible inside the cirrata tubes of P. mandela n. sp. (see Fig. 7 D), resembling the epidermal droplets recently described for Ptychostomella lamelliphora Todaro, 2013 (see Todaro 2013, Fig. 4 D), seem to support this hypothesis. The reported disparities between juveniles and adults highlight the significant ontogenetic morphological variations experienced by Pseudostomella specimens during their life, and once again caution researchers on using only mature specimens for a reliable identification and/or species description. Taxonomic affinities. Within Thaumastodermatinae, the genera Tetranchyroderma and Pseudostomella, the number of prongs forming the peculiar scales called ancres, which composes the body cuticular armature, has been regarded as the single most useful taxonomic trait to classify species (e.g., Lee & Chang 2002; Todaro 2002; but see Todaro et al. 2011 a). Consequently, in the genus Pseudostomella three basic species groups are envisaged based on the type of pronged spines i.e., species characterized by triancres (3 prongs), tetrancres (4 prongs) or pentancres (5 prongs). Based on the type of ancres, Pseudostomella mandela n. sp. approaches six other species all characterized by a tetrancrous covering: P. andamanica Rao, 1993, P. indi ca Rao, 1970, P. koreana Lee & Chang, 2002, P. longifurca Lee & Chang, 2002, P. m al ay i ca Renaud-Mornant, 1967 and P. ro s c o vi t a Swedmark, 1956 (see Todaro 2012). However, based on the number of dorsal papillae (5) on the preoral palps, the new species is most similar to P. longifurca and P. indica. The number and distribution of the adhesive tubes is useful in discriminating the three taxa e.g., P. longifurca bears 5 TbA and 7 TbP per side and P. i n di c a 2 TbA and 5 TbP, in contrast with the new species that exhibits 4 TbA and 4 TbP per side. P. mandela n. sp. is further distinguished as the only species in the genus that possesses cirrata tubes (7 pairs). The finding of an additional new taxon seems to support the idea that Pseudostomella species appear to have a relatively restricted geographic range, at least compared to the wide distribution and cosmopolitan nature of many other gastrotrichs (cf. Todaro et al. 1996; Artois et al. 2011; Curini-Galletti et al. 2012; Kånneby et al. 2012; Kieneke et al. 2012).Published as part of Todaro, M. Antonio, Perissinotto, Renzo & Bownes, Sarah J., 2015, Two new marine Gastrotricha from the Indian Ocean coast of South Africa, pp. 193-208 in Zootaxa 3905 (2) on pages 200-205, DOI: 10.11646/zootaxa.3905.2.2, http://zenodo.org/record/23214

Dactylopodola nadine Todaro, Perissinotto & Bownes, 2015, n. sp.

Dactylopodola nadine n. sp. Figs. 1–5 ZooBank lsid:zoobank.org:act: 64 E 36 F 93 - DFF 3-44 A 4 -A0C 5-4257310 AB 6 BE Type locality. South Africa, KwaZulu-Natal, Cape Vidal, iSimangaliso Wetland Park (Latitude 28 °07’ 18 ” S; Longitude 32 ° 33 ’ 43 ” W); about 2.5 m water depth in fine to very fine well sorted sand (mean grain size, 0.225 mm, sorting, 0.43). Values of salinity and pH of coastal waters around the time of sampling were 36.8 and 8.4, respectively, with temperatures ranging from 27 to 28 ° C. Type specimens. Holotype: the 227 Μm long adult specimen shown in Figure 2, no longer extant (International Code of Zoological Nomenclature, Articles 73.1. 1 and 73.1.4), collected on 12 February 2013 (MAT legit). Additional material examined. Four adults and one subadult specimen, all collected by the first author from the type locality, all were observed alive and are no longer extant. Four additional identified specimens were fixed in alcohol and are kept in the collection of the first author. Ecology. Frequency of occurrence: common in sediment outside the wave-breakers along the ocean shore of the iSimangaliso Wetland Park. Abundance: numerous in sub-littoral sediment at 2.5 m where found. Diagnosis. A Dactylopodola, up to 230 Μm in length; PhIJ at U 24; head rounded, with medial bulge slightly forward, body well partitioned into head/neck/trunk/caudum regions. Sensory hairs: sparse, but more numerous on head especially its lateral surfaces, occurring in dorsolateral columns down the body length. Epidermal glands absent. Adhesive tubes: TbA, 3 per side, of different length; TbL arranged as 1 + 1 + 2; TbP, 4 per side, 2 arising distally from caudal lobes and 2 arising laterally on each side in front of these. Ventral locomotory ciliation: longitudinal field running nearly the whole length of the body, split throughout the intestinal region. Reproductive system: protandrous, simultaneous or alternating hermaphrodites; testes paired in mid-intestinal region; ovaries paired in posterior intestinal region, eggs developing toward the anterior in a more medial position. glandular caudal organ embracing the terminal portion of the intestine; frontal organ or allosperm not visible. Etymology. The species is dedicated to the late Nadine Gordimer, South African writer, civil right activist and recipient of the 1991 Nobel Prize in Literature. Description. The description is based mostly on the adult holotype specimen of 227 Μm in total length. Head rounded anteriorly, with a slight medial bulge forward in conjunction with the mouth; body well-delineated into head/neck/trunk/caudum regions; widths of head\neck\trunk\caudal base 30 \ 19 \ 28 \ 14 µm at U 10 \U 22 \U 57 \U 87, respectively. The Caudum consists of a relatively short, broad peduncle that ends in paired lobes that indent medially to U 92. Head bears numerous sensory hairs of mixed length (6–15 µm), most occurring laterally; other sensory hairs occur in dorso-lateral columns from U 14 to U86, 8– 10 evenly-spaced hairs per side (8–13 µm in length). Epidermal glands not noted. Longitudinal muscles are visibly striated, which is characteristic of members of this family. Adhesive tubes. TbA, 3 per side, inserting directly on the body surface and radiating from a more-or-less common base at U 11; one shorter (8 Μm in length) inserted more medially and two longer (11–12 µm in length) projecting laterally. TbL, 5 per side, arranged as 1 + 1 + 2 at U 35, U 46, U 61 and U 66 respectively; the lengths of the first two tubes are 13–15 Μm, while the lengths of the final two tubes are progressively shorter (11 – 9 Μm). TbP, 4 per side, two arising distally from the caudal lobes (10–12 µm in length) and two arising laterally on each side in front of these (8–9 Μm in length). Ventral ciliation. A longitudinal field of sparse cilia extends from U05 to U 92, splitting into two bands throughout the intestinal region, U 22 -U 80, and eventually forming separated tufts posterior to the anus; individual cilia of the bands are 10–20 µm in length. Digestive tract. Mouth of medium size (ca. 5.5 Μm in diameter), projecting very slightly ventrally and leading progressively into a 53 Μm long pharynx measured from the anterior margin of the mouth to the pharyngeointestinal junction; pharynx muscular, roughly cylindrical (12 Μm in diameter), showing pharyngeal pores near the base, at U 22; pharynx connected to sac-like intestine at pharyngeo-intestinal junction at U 25; intestine straight, narrowing posteriorly, anus ventral at U 80. Reproductive tract. Protandrous, simultaneous or alternating hermaphrodites; testes occur as irregular, paired clusters of spindle-like spermatocytes in the midintestinal region, measuring 55–62 µm in length by 6–14 µm in width, with individual cells approximately 1 µm in length yielding several tens per side; ovaries are paired in the posterior intestinal region, with one or two maturing eggs attaining their development by shifting anteriorly and dorsally in a more medial position; Glandular caudal organ (about 17 Μm in length) embracing the terminal portion of the intestine; frontal organ or allosperm not seen (absent). Variability and remarks. The body length of the other four adult specimens was very similar: mean = 476.6 µm, SD = 5.3 µm. Two specimens exhibited both testes filled with sperm and a fairly large caudal organ but with immature eggs inside; the other two specimens had no sperm in the testes and a smaller caudal organ and a large, mature egg dorsal to the posterior intestine (Figure 4). Other characteristics matched those reported for the holotype. The studied subadult (Figure 5) was 186 µm in TL and possessed a full set of adhesive tubes i.e., 3 TbA, 1 + 1 + 2 TbL and 4 TbP. Taxonomic affinities. According to the recently updated key to the genus Dactylopodola, there are currently nine formally recognized (described) species worldwide (Gilsa et al. 2014). Among these, D. nadine n. sp. is most similar to D. baltica and D. roscovita in that it also bears eye-spots. However, the new species can easily be distinguished from the latter two species by its smaller size (LT = 230 Μm vs 275 Μm and 450 Μm, respectively) and by the lower number of adhesive tubes of the anterior, lateral and posterior series (on each side: 3, 4 and 4 vs 5, 6 and 8 and 2, 9 and 12–15, respectively). In terms of body size, presence of eye spots, and number and distribution of adhesive tubes, D. nadine n. sp. is extremely similar to D. cf baltica, which was found by the first author in the Arabian Gulf (Kuwait). The 18 rRNA gene sequence of D. cf baltica (GenBank accession code JF 357650) has been included in several phylogenetic studies of Gastrotricha (e.g., Todaro et al. 2011 a, 2012 a, 2014), thus future comparisons based on molecular markers may reveal the relationships between these two taxa.Published as part of Todaro, M. Antonio, Perissinotto, Renzo & Bownes, Sarah J., 2015, Two new marine Gastrotricha from the Indian Ocean coast of South Africa, pp. 193-208 in Zootaxa 3905 (2) on pages 196-199, DOI: 10.11646/zootaxa.3905.2.2, http://zenodo.org/record/23214

Scottish archaeological radiocarbon dates associated with The National Museums Scotland, 2019/20

No abstract available