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Whitfield Et Al. 2017.Pdf Biological Conservation 212 (2017) 256–264 Contents lists available at ScienceDirect Biological Conservation journal homepage: www.elsevier.com/locate/biocon Life-histories explain the conservation status of two estuary-associated MARK pipefishes ⁎ Alan K. Whitfielda, , Thomas K. Mkareb,1, Peter R. Teskeb, Nicola C. Jamesa, Paul D. Cowleya a South African Institute for Aquatic Biodiversity (SAIAB), Private Bag 1015, Grahamstown 6140, South Africa b Molecular Zoology Laboratory, Department of Zoology, University of Johannesburg, Aukland Park 2006, South Africa ABSTRACT Two endemic southern African pipefish species (Teleostei: Syngnathidae) co-occur in estuaries on the southeast coast of South Africa. The larger longsnout pipefish, Syngnathus temminckii, is abundant and has a wide range that comprises coastal and estuarine habitats in all three of the region's marine biogeographic provinces. In contrast, the smaller estuarine pipefish S. watermeyeri is critically endangered, and confined to a few warm- temperate estuaries. Here, we explore reasons for these considerable differences in conservation status. Fecundity is related to fish size, with large live-bearing S. temminckii males carrying up to 486 developing eggs/ embryos, compared to a maximum of only 44 recorded for S. watermeyeri. Loss of submerged seagrass habitats due to episodic river flooding appears to be correlated with the temporary absence of both species from such systems. Prolonged cessation in river flow to estuaries can cause a collapse in estuarine zooplankton stocks, a food resource that is important to pipefish species. The greater success of S. temminckii when compared to S. watermeyeri can be attributed to the former species' wider geographic distribution, fecundity, habitat selection and ability to use both estuaries and the marine environment as nursery areas. Genetic data indicate that this has resulted in a much smaller long-term effective population size of S. watermeyeri, a situation that has persisted since the beginning of the present interglacial period. Syngnathus watermeyeri is thus naturally more susceptible to anthropogenic disturbances, which have resulted in an alarming reduction in its contemporary population size. Possible measures to promote the conservation of S. watermeyeri are presented. 1. Introduction species at an advantage over the latter. Syngnathus temminckii and S. watermeyeri have a conservation status Fishes have over 30 reproductive guilds that can essentially be di- that also differs considerably between the two species. The former is vided into three main categories, namely non-guarders, guarders and common within its South African distributional range, from the cool bearers (Balon, 1975). Pipefishes belong to the bearer category and temperate west coast, through the estuaries and marine environment of more specifically the external bearers. Typically they exhibit parental the warm temperate southern and south-eastern coasts, reaching into care, have a low fecundity but invest a large amount of energy in each the subtropical zone on the east coast (Mwale et al., 2014). In contrast, of a small number of well-developed precocial young. The adults of S. watermeyeri has been recorded in only a limited number of estuaries such species are often specialists, have a narrow trophic niche and on the warm temperate south-east coast and, even in those estuaries, usually live in a stable and predictable environment (Bruton, 1989). the numbers are generally very low (Whitfield, 1995). Although the longsnout pipefish Syngnathus temminckii Kaup, 1856 More recently, S. watermeyeri has been listed as Critically and the estuarine pipefish S. watermeyeri Smith, 1963 fulfil many of the Endangered (CR) in the IUCN Red List (www.iucnredlist.org). The main criteria outlined above, both species occur in estuaries that are gen- threats to its existence are habitat loss, river degradation and loss of erally unstable and unpredictable environments (Whitfield, 1990). freshwater inputs to estuaries (Vorwerk et al., 2007). River inflow Fortunately for S. temminckii, it also occurs in the marine environment provides the nutrients required to stimulate planktonic productivity in that is much more stable and predictable, thus conferring this species estuaries (Grange et al., 2000), the food chain upon which this species with a distinct advantage over S. watermeyeri. This study will show that depends for its survival (Whitfield, 1995). Loss of river pulses due to this is but one of the many life-history traits that places the former excessive freshwater abstraction in the catchments leads to a reduction ⁎ Corresponding author. E-mail address: a.whitfi[email protected] (A.K. Whitfield). 1 Present address: Kenya Marine and Fisheries Research Institute, P.O. Box 81651, Mombasa 80100, Kenya. http://dx.doi.org/10.1016/j.biocon.2017.06.024 Received 3 October 2016; Received in revised form 2 June 2017; Accepted 15 June 2017 0006-3207/ © 2017 Elsevier Ltd. All rights reserved. fi A.K. Whit eld et al. Biological Conservation 212 (2017) 256–264 in estuarine zooplanktonic resources (Froneman and Vorwerk, 2013), Bushmans and the East Kleinemonde estuaries in the Eastern Cape with dire consequences for an endangered species such as S. water- Province (Whitfield, 1995; Fig. 1), spanning a coastal distance of only meyeri. 60 km. The main aim of this paper is to examine the life-history styles and The type specimens of S. watermeyeri were collected in the Kariega population dynamics of S. temminckii and S. watermeyeri in the East Estuary during the early 1960s, but by the 1980s and 1990s this species Kleinemonde and Kariega estuaries and to equate these findings with had disappeared from that system (Whitfield and Bruton, 1996), only to the current conservation status of the two species. We use modern reappear in 2006 following river flushing of the estuary (Vorwerk et al., molecular techniques in our analysis of the population genetics of these 2007 ). It is important to note that S. temminckii remained present syngnathids (Mobley et al., 2011) and hypothesise that the long-term throughout and was sometimes abundant in the Kariega Estuary during effective population sizes of these two species should reflect their pre- the decades when S. watermeyeri was locally extinct in that system (Ter sent IUCN categorization. This would imply that S. watermeyeri, which Morshuizen and Whitfield, 1994; Whitfield and Bruton, 1996). It should is of major conservation concern, already had a smaller population size also be noted that S. temminckii has also been recorded from estuaries under natural conditions that made it particularly vulnerable to con- where submerged aquatic macrophyte beds are absent (Mwale et al., temporary habitat disturbances. Finally, we attempt to link the life- 2014). history cycles of the two pipefish species to their current status in the Both S. temminckii and S. watermeyeri have been recorded in Zostera wild, with S. temminckii showing all the attributes of a successful coastal capensis and Ruppia cirrhosa plant beds within the Kariega and East species, whereas the closely related S. watermeyeri is at considerable Kleinemonde estuaries, respectively (Fig. 1). Indeed, the type specimens risk of extinction (Whitfield and Bruton, 1996). of S. watermeyeri were captured together with S. temminckii individuals from the same eelgrass bed in 1963 (D. Galpin, pers. comm.). In es- 1.1. Study species tuarine systems elsewhere in South Africa where submerged plant beds are present, S. temminckii usually occurs on its own, although other fi Syngnathus temminckii and S. watermeyeri are two southern African pipe sh species (e.g. Hippichthys spicifer) are sometimes also recorded fi representatives of the pipefish genus Syngnathus. The former species is from these habitats (Harrison and Whit eld, 2006). The juveniles and the more abundant and widely distributed of the two, occurring in adults of both Syngnathus species are normally associated with sub- coastal waters (including estuaries) from cool-temperate Walvis Bay in merged seagrass beds in certain Eastern Cape |Province estuaries, with Namibia to subtropical waters along the east coast of South Africa S. temminckii also being associated with seaweed and reef habitats in the (Heemstra and Heemstra, 2004). In contrast, the latter species is rare coastal marine environment. and restricted to a few estuaries on the subcontinent between the Syngnathus temminckii in southern African waters was previously Fig. 1. Published sites of occurrence for Syngnathus temminckii (•) and S. watermeyeri (*) in southern Africa (map modified from Mwale et al., 2014). The boundaries of the three estuarine biogeographic zones along the South African coast are also shown. 257 fi A.K. Whit eld et al. Biological Conservation 212 (2017) 256–264 misidentified as Syngnathus acus Linnaeus, 1758, but a detailed mor- (December, January or February) and winter (June, July or August) phological and genetic study of the species (Mwale et al., 2013) con- from December 1994 to July 2014 (sampling methods are described in firmed that it was in fact S. temminckii. The snout of this species is a detail by James et al., 2008). The estuary was divided longitudinally distinguishing feature when compared to S. watermeyeri, with the into lower, middle and upper reaches, with up to 18 sites sampled on former having a snout longer than the rest of the head whereas the each occasion. A small mesh (5 mm bar) seine net (30 m × 2 m) was latter species has a snout one third of its corresponding head length
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