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Hydrobiologia (2011) 678:17–36 DOI 10.1007/s10750-011-0810-5

PRIMARY RESEARCH PAPER

Freshwater mussel (Mollusca: Bivalvia: Unionoida) richness and endemism in the ecoregions of Africa and Madagascar based on comprehensive museum sampling Daniel L. Graf • Kevin S. Cummings

Received: 10 January 2011 / Revised: 20 June 2011 / Accepted: 25 June 2011 / Published online: 3 August 2011 Springer Science+Business Media B.V. 2011

Abstract The objective of this study was to assess freshwater mussel (Mollusca: Bivalvia: Unionoida) species distributions among the freshwater ecoregions of Africa and Madagascar to discover areas of high richness and endemism. These are among the top criteria for identifying biodiversity hotspots and establishing conservation priorities. Distributions were determined from museum specimens in 17 collections. In total, 5,612 records for 87 unionoid species could each be assigned to one of 90 freshwater ecoregions. The majority of species (55%) are known from only one (34 spp.) or two (14) ecoregions. Only three are known from more than 20 ecoregions: Etheria elliptica (38 ecoregions), Chambardia wahlbergi (25), and Mutela rostrata (21). The most species-rich ecoregions are Lake Victoria Basin (17 spp.), Upper Nile (16), Upper

Handling editor: Koen Martens

Electronic supplementary material The online version of this article (doi:10.1007/s10750-011-0810-5) contains supplementary material, which is available to authorized users. D. L. Graf (&) Department of Biological Sciences, University of Alabama, Tuscaloosa, AL 35487, USA e-mail: [email protected] K. S. Cummings Illinois Natural History Survey, University of Illinois, Champaign, IL 61820, USA

Congo (14), Senegal–Gambia (13), and Sudanic Congo–Oubangi (13). Those with the most endemic species are Lake Tanganyika (8 spp.), Lake Victoria Basin (6), Bangweulu–Mweru (4), and Lake Malawi (3). Twenty-five ecoregions have no known freshwater mussels. These patterns are significantly correlated with fish and general freshwater mollusk richness. Unionoid richness also varies significantly among major habitat types. These patterns are relevant to biogeography and conservation and indicate areas in need of further research. We argue that freshwater mussels are valuable as focal species for conservation assessments, and they themselves merit management consideration for their ecosystem functions and distributions in imperiled habitats. It is recommended that field surveys be conducted to determine the current status of species in all areas of Africa and Madagascar. Keywords Unionidae Iridinidae Etheriidae Margaritiferidae Africa Madagascar Ecoregions

Introduction The freshwater mollusks of Africa and Madagascar are a species-rich and heterogeneous assemblage of both gastropods (Brown, 1994) and bivalves (Mandahl-Barth, 1988; Daget, 1998). These taxa are of practical interest, not merely as constituents of Afrotropical natural heritage, but also for the insights

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they allow into the historical and contemporary forces impinging on the lakes and rivers of the region—a threatened resource with a dependent biota (Jackson et al., 2001; Johnson et al., 2001; Lehner, 2005; Dudgeon et al., 2006; Strayer & Dudgeon, 2010; Woodward et al., 2010). Bivalves of the order Unionoida, known as freshwater mussels, are imperiled globally (Lydeard et al., 2004; Strayer, 2006), but their distributions and conservation status are incompletely understood in Africa (see Seddon et al., 2011, for a review). Approximately 90 species have been recognized from the Afrotropics (Graf & Cummings, 2007a, 2009) and the Palearctic northwestern African Maghreb (Araujo et al., 2009a). The objective of this study is to provide a comprehensive ecoregion-based assessment of the freshwater mussel species distributions in Africa and Madagascar to (1) discover areas of high species richness and endemism, and (2) evaluate the congruence of the patterns observed with those of other freshwater taxa and major habitat types. These species-based patterns are among the top criteria for identifying biodiversity hotspots and conservation areas (Reid, 1998; Mace, 2004; Darwall & Vie´, 2005). Thieme et al. (2005) and Abell et al. (2008) partitioned the fresh waters of Africa, Madagascar, and associated islands into 90 freshwater ecoregions (Fig. 1; Table 1). According to Abell et al. (2002, p. 19), an ecoregion is ‘‘a relatively large area of land or water containing a geographically distinct cluster of natural communities. These communities (a) share a large majority of their species and ecological dynamics, (b) share similar environmental conditions, and (c) interact ecologically in ways that are critical for their long-term persistence.’’ Freshwater ecoregions generally conform to watersheds or segments of larger basins. The general merits of a watershedversus an ecoregion-based description of aquatic landscape heterogeneity have been debated elsewhere (Omernik & Baily, 1997; Zogaris et al., 2009). Although a variety of aquatic taxa (including mollusks) contributed to the determination of ecoregion boundaries, the emphasis fell overwhelmingly on the ichthyofauna. This is not surprising given the precedents set in Afrotropical biogeography (Roberts, 1975; Beadle, 1981; Le´veˆque, 1997), the centrality of fisheries to Africa’s economy (Heck et al., 2007), high species richness (Lundberg et al., 2000), and an impressive array of experts and infrastructure capable

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of supporting a contemporary and authoritative continent-wide review (Abell et al., 2008). Despite this bias, the ecoregions provide a valuable framework for analyses of freshwater taxa generally. For us, they are useful in that they have already been defined, the scale is appropriate for aggregating relatively sparse collection localities, and a large dataset has already been assembled for other taxa (Thieme et al., 2005). As a result of similar habitat requirements and because freshwater mussel larvae are obligate parasites of freshwater fishes (Watters, 1994; Wa¨chtler et al., 2001; but see Kondo, 1990), we predict that the distributions of these two taxa should be highly correlated. Little is known about the host–parasite relationships among African taxa, but the phylogenetic distribution of this trait confirms the generality of this association among the species in this study (Graf & Cummings, 2006a). Even without precise knowledge of host–parasite relationships, it has been well documented in other areas that patterns of fish and mussel richness are not independent (Watters, 1992; Vaughn & Taylor, 2000). The species-level taxonomy of freshwater mussels in Africa and Madagascar is relatively well documented compared to other tropic regions. There have been four recent species-level inventories: Haas (1969), Mandahl-Barth (1988), Daget (1998), and Graf & Cummings (2007a). However, these reviews are insufficiently precise in their summaries of species’ ranges to accurately determine ecoregion occurrence, especially for widespread species. For example, according to Daget (1998, p. 149), Mutela rostrata is found in the ‘‘bassins du Seńe´gal, Niger, Tchad, Nil et Zaı¨re, lacs Albert et Mweru (Moero), jusqu’a` Lourenzo-Marque`s.’’ It is unreasonable to assume that this mollusk has been observed to occur in every ecoregion fitting that vague description. Yet, these are the data that have, by necessity, been relied upon for previous conservation assessments (Seddon et al., 2011). A thorough review of the primary literature would increase the resolution and capture the extent of our published knowledge, but the utility would be compromised by ambiguity resulting from the disparate taxonomic systems applied over the last 250? years (Bortolus, 2008). Instead, we have focused upon the museum specimens (i.e., vouchers) that form the ultimate bases of both known distribution and taxonomy.


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Fig. 1 The freshwater ecoregions of Africa and Madagascar. Numerical keys are listed in Table 1

Materials and methods Specimens from 17 research museums in the United States, Europe, and Australia were sampled from December 2002 to December 2009 (Table 2) as part of a larger project to create a database for freshwater mussel families on the southern continents. Each specimen lot was digitally photographed to document shell morphology and original label information. Textual data (catalog number, previous identifications, collection locality, etc.) were recorded simultaneously or captured subsequently from the images.

For northwestern Africa (Maghreb), we relied on the recent literature (Araujo et al., 2009a, b, c) to augment our museum work, as Palearctic taxa were beyond the scope of our collections sampling. The MUSSEL Project Database (MUSSELpdb) was developed in FileMaker Pro (FileMaker, Inc., Santa Clara, USA) to handle freshwater mussel specimen records as well as species-, genus-, and family-group level taxonomy and bibliographic data. Each specimen record was assigned geocodes varying in precision from specific localities to nearby towns, river basins, or larger political divisions. Geocodes

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Table 1 Freshwater ecoregions of Africa and Madagascar

Table 1 continued

501 Atlantic Northwest Africa

547 Mai Ndombe

502 Mediterranean Northwest Africa

548 Malebo Pool

503 Sahara

549 Lower Congo Rapids

504 Dry Sahel

550 Lower Congo

505 Lower Niger–Benue

551 Cuanza

506 Niger Delta

552 Namib

507 Upper Niger

553 Etosha

508 Inner Niger Delta 509 Senegal–Gambia

554 Karstveld Sink Holes 555 Zambezian Headwaters

510 Fouta–Djalon

556 Upper Zambezi Floodplains

511 Northern Upper Guinea

557 Kafue

512 Southern Upper Guinea

558 Middle Zambezi–Luangwa

513 Mount Nimba

559 Lake Malawi

514 Eburneo

560 Zambezian Highveld

515 Ashanti 516 Volta

561 Lower Zambezi

517 Bight Drainages

563 Eastern Zimbabwe Highlands

518 Northern Gulf of Guinea Drainages

564 Coastal East Africa

519 Western Equatorial Crater Lakes

565 Lake Rukwa

520 Lake Chad

566 Southern Eastern Rift

521 Lake Victoria Basin

567 Tana, Athi, & Coastal Drainages

522 Upper Nile

568 Pangani

523 Lower Nile 524 Nile Delta

569 Okavango 570 Kalahari

525 Ethiopian Highlands

571 Southern Kalahari

526 Lake Tana

572 Western Orange

527 Western Red Sea Drainages

573 Karoo

528 Northern Eastern Rift

574 Drakensberg–Maloti Highlands

529 Horn of Africa

575 Southern Temperate Highveld

530 Lake Turkana

576 Zambezian Lowveld

531 Shebelle–Juba 532 Ogooue–Nyanga–Kouilou–Niari

577 Amatolo–Winterberg Highlands

533 Southern Gulf of Guinea Drainages–Bioko

579 Western Madagascar

534 Sangha

580 Northwestern Madagascar

535 Sudanic Congo–Oubangi

581 Madagascar Eastern Highlands

536 Uele

582 Southern Madagascar

537 Cuvette Centrale

583 Madagascar Eastern Lowlands

538 Tumba 539 Upper Congo Rapids

584 Comoros–Mayotte 585 Seychelles

540 Upper Congo

586 Mascarenes

541 Albertine Highlands

587 Sao Tome & Principe–Annobon

542 Lake Tanganyika

902 Cape Verde Islands

543 Malagarasi–Moyowosi

903 Canary Islands

544 Bangweulu–Mweru

905 Socotra

545 Upper Lualaba

Numerical keys as per Abell et al. (2008)

546 Kasai

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562 Mulanje

578 Cape Fold


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Table 2 Mollusk collections visited from 2003 to 2009 Collection MRAC

Location

Georeferenced lots 1185 (1274)

Tervuren Belgium

12/2009

Paris France

05/2006, 11/2006

930 (1110)

Brussels Belgium London UK

12/2009 11/2004

744 (904) 615 (790)

ZMB

Royal Belgian Institute of Natural Sciences (British) Natural History Museum Museum fu¨r Naturkunde

Berlin Germany

01/2006

374 (486)

SMF

Senckenberg Museum

Frankfurt Germany

07/2008

342 (412)

ANSP

Academy of Natural Sciences

Philadelphia USA

2003–2008*

340 (398)

MCZ

Museum of Comparative Zoology

Cambridge USA

01/2003, 04/2004

336 (350)

MNHN IRSNB BMNH

Royal Museum of Central Africa Museúm National d’Histoire Naturelle

Dates

UMMZ

University of Michigan Museum of Zoology

Ann Arbor USA

2003–2008*

278 (327)

USNM

National Museum of Natural History

Washington USA

11–12/2005

241 (279)

AMNH

American Museum of Natural History

New York USA

04/2005

87 (118)

FMNH

Field Museum of Natural History

Chicago USA

2003–2008*

68 (79)

CM

Carnegie Museum of Natural History

Pittsburgh USA

10/2003, 09/2004

21 (31)

DMNH

Delaware Museum of Natural History

Wilmington USA

05/2005

21 (30)

AMS

Australian Museum

Sydney Australia

07/2004

17 (29)

INHS

Illinois Natural History Survey

Champaign USA

08/2004

10 (12)

SBMNH

Santa Barbara Museum of Natural History

Santa Barbara USA

02/2005 Total

3 (3) 5612 (6632)

Only those records that could be georeferenced with sufficient precision to place them in a single ecoregion were used for our analyses. The total numbers of specimen lots examined from each collection are listed parenthetically in the last column * ANSP, UMMZ and FMNH specimens were at hand or on loan for an extended period

were obtained from NGA GEOnet Names Server (GNS; http://earth-info.nga.mil/gns/html/) as well as the Fuzzy Gazetteer (FuzzyG; http://tomcat-dma web1.jrc.it/fuzzyg/query/), the georeferenced placenames published in Pilsbry (1919, pp. 11–21) and Pilsbry & Bequaert (1927, pp. 76–85), specimen labels, and other sources. Except when prohibited by imprecision, each locality was assigned to a single ecoregion (Table 1). Geocodes were confirmed with GoogleMaps (http://maps.google.com/), and ecoregion assignments were verified using iMap 3.5 (Biovolution, Leuven, Belgium) to plot localities on an equidistant cylindrical projection (Fig. 1). The ecoregions of Africa and Madagascar are indicated using a numerical key established by Abell et al. (2008) [501–587, 902–903, 905]. When we refer to an ecoregion, its key is provided in square brackets. There is not a perfect correspondence between the ecoregions of Abell et al. (2008) and Thieme et al. (2005). In a single case, one of the ecoregions of Thieme et al. (2005), Permanent Maghreb, was divided by Abell et al. (2008): Atlantic

Northwest Africa [501] and Mediterranean Northwest Africa [502]. For comparisons with previous taxon assessments, we applied the union of our dataset for these two ecoregions (referred to as [501–502]). Four smaller ecoregions were combined with larger adjacent ones by Abell et al. (2008) (see Electronic Supplementary Material associated with this article). Taxonomy follows the global checklist of Graf & Cummings (2007a), updated by Graf & Cummings (2009) for Madagascar and Araujo et al. (2009a, b, c) for the Palearctic Maghreb. Higher taxonomy is based on Graf & Cummings (2006a), except that Germainaia geayi is regarded as incertae sedis at the family level. For each ecoregion, we tallied the numbers of museum lots, collecting localities, total species (i.e., richness), and endemics. We did not include species represented only by fossils or subfossils (e.g., specimens missing periostracum; rebut = poor quality shells or fragments). Endemics were counted by two different criteria: (1) species that occur in only a single ecoregion, and (2) those restricted to only two adjacent ecoregions.

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To assess the value of the patterns of unionoid species richness and endemism for predicting overall aquatic diversity, we tested their correlations with the richness of fishes as well as other freshwater mollusks (i.e., gastropods and veneroid bivalves). Fish data were from Thieme et al. (2005), but the mollusk counts were determined from their original database (T.K. Kristensen, unpubl.) to remove freshwater mussels from the aggregated mollusk totals. Their mollusk database lacked records for Madagascar, and so those ecoregions were not analyzed. Linear regressions were performed and the best-fit line (ordinary least-squares), Pearson coefficient (r), and P-value were determined using PAST: PAlaeontological STatistics (Hammer et al., 2001; http://folk.uio.no/ohammer/past/). Outliers were determined based on the residuals at the 95% level. Thieme et al. (2005) also assigned ecoregions to major habitat types. To test the hypothesis that species richness varies according to habitat type, we applied a Kruskal–Wallis Test in PAST (Hammer et al., 2001). The null hypothesis was that the median richness for each major habitat type was the same. This was followed by Bonferroni-corrected Mann– Whitney (Wilcoxon) pairwise tests. All specimen records are available at http://www. mussel-project.net/, and information about supporting vouchers and other notes are provided in the Electronic Supplementary Materials associated with this article.

Results Examination of museum holdings yielded 6,632 relevant specimen lots, and 5,612 (85%) could be assigned to ecoregions in Africa or Madagascar (Table 2). More than 60% of georeferenced voucher lots (3,474 lots) came from only four museums: MRAC (1185), MNHN (930), IRSNB (744), and BMNH (615). The next tier of collections (ZMB, SMF, ANSP, MCZ, UMMZ, and USNM) each contributed from 278 to 374 georeferenced specieslocality records, and the remaining 227 records came from the other seven collections, for which Africa has not been a major research focus. Historical sampling success varied among ecoregions (Fig. 2a). A mere ten ecoregions (11%) account for 71% of our data (3,984 lots), with noticeable

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peaks in Senegal–Gambia [509], Upper Nile [522] (and adjacent ecoregions), Lake Tanganyika [542], Bangweulu–Mweru [544], and Lake Malawi [559]. Three ecoregions are represented by only a single collecting locality each, and 26 more had no museum records. Where possible, we have augmented our collections data with published records (e.g., Germain, 1925; Connolly, 1939; Appleton, 1979, 1996). Germain (1907) reported Etheria elliptica from the Androtsy River, and this is the sole record representing a freshwater mussel in Southern Madagascar [582]. Examination of museum specimens failed to distinguish three species currently regarded as valid, and we added a single, previously omitted species. The taxa that we could not distinguish belong to the ‘‘Aspatharia chaiziana species complex.’’ Whereas Mandahl-Barth (1988) recognized only a single species (A. chaiziana), Daget (1998) reported six: A. chaiziana, A. mabillei, A. pangallensis, A. rochebrunei, A. tawaii, and A. tristis. We were unable to distinguish A. tawaii from A. chaiziana, A. pangallensis from A. mabillei, and A. tristis from A. rochebrunei. We therefore combined data for the species in each pair. Leguminaia saulcyi (Bourguignat, 1852) has generally been considered to be restricted to Syria and the Orontes River (Schu¨tt, 1983; Falkner, 1994; Graf, 2007). However, a synonym of this species was described from Libya (Unio tripolitanus Bourguignat, 1852), and we have added L. saulcyi to our species list. Otherwise, we maintained the current consensus classification (Table 3). Details of species occurrence, voucher specimens, and associated notes for each ecoregion are included in the Electronic Supplementary Material. Of the 87 freshwater mussel species recognized in this study, two were not assigned to any ecoregion: Coelatura rothschildi and G. geayi. The former species is known only as fossils/subfossils in Lake Turkana (Daget, 1998; Graf & Cummings, 2007b). G. geayi is known from only a single lot allegedly from Madagascar (Graf & Cummings, 2009), but the locality is imprecise. Most species (55%) have relatively small ranges, occurring in only one (34 spp.) or two (14) ecoregions, although three species occur in [20 (Fig. 3). The number of species per ecoregion ranges from 0 to 17 (median 3.5; Fig. 2b). Seventy-two percent of


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Fig. 2 Museum lots (a) and species richness (b) by ecoregion. Ecoregions with outstanding numbers of museum vouchers are indicated by their numerical key (Table 1)

the ecoregions have at least one species; there are 25 ecoregions without known freshwater mussels (Fig. 4). Lake Victoria Basin [521] and the adjacent Upper Nile [522] have the highest species richness. Richness in general is the highest in the tropical ecoregions of western and central Africa, including the upper Nile Basin (Fig. 5a). Figure 5b depicts areas of endemism—those ecoregions inhabited by species with small ranges (i.e., two or fewer ecoregions). The ecoregion distributions of 48 species with small ranges are listed in Table 4. When only single-ecoregion endemics are considered, Lake Tanganyika [542], Lake Victoria Basin [521], and Bangweulu–Mweru [544] have the top three endemic richness values (in that order). However, when species restricted to B2 ecoregions are considered, Lake Victoria Basin [521] has the highest endemic richness due to the taxa shared with Lake Albert in the adjacent Upper Nile [522]. Freshwater mussel richness and endemism are significantly correlated with fish richness and endemism, as well as general freshwater mollusk (nonunionoid) richness and endemism (Fig. 6). Thieme et al. (2005) characterized each of the freshwater ecoregions by their dominant (terrestrial) habitat type. Freshwater mussel species richness varies significantly across major habitat types, with

xeric systems (XS), highland and mountain streams (HMS), and island rivers and lakes (IRL) each having significantly lower median richness than moist forest rivers (MFR) and/or savanna–dry forest rivers (SDFR) (Fig. 7).

Discussion Data quality We have assembled a comprehensive dataset on the diversity and distributions of Afrotropical freshwater mussel species. However, the synthesis of 5,612 georeferenced museum lots made in this study falls short of perfection. To make quantitative comparisons of richness and endemism based on previous sampling, it is necessary to assume that equivalent (or at least sufficient) effort was expended in each ecoregion. Unfortunately, the nature of the presenceonly museum records employed herein does not support this. The lack of records on oceanic islands like Seychelles [585] or in xeric habitats such as Kalahari [570] surely indicates a true absence of freshwater mussels, and, the large numbers of museum lots from Senegal–Gambia [509], Lake Victoria Basin [521], and Lake Tanganyika [542]

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Table 3 Freshwater mussels (Unionoida) of Africa and Madagascar

Table 3 continued

FAMILY UNIONIDAE

45 Margaritifera marocana (Pallary, 1918)

1 Anodonta anatina (Linnaeus, 1758)

FAMILY IRIDINIDAE

2 Anodonta cygnea (Linnaeus, 1758)

46 Aspatharia chaiziana ? A. tawaii (Rang, 1835)

3 Brazzaea anceyi Bourguignat, 1885

47 Aspatharia dahomeyensis (Lea,1859)

FAMILY MARGARITIFERIDAE

4 Cafferia caffra (Krauss, 1848)

48 Aspatharia divaricata (von Martens, 1897)

5 Coelatura aegyptiaca (Cailliaud, 1827)

49 Aspatharia droueti (Chaper, 1885)

6 Coelatura alluaudi (Dautzenberg, 1908) 7 Coelatura bakeri (H. Adams, 1866)

50 Aspatharia mabillei (Jousseaume, 1886) ? A. pangallensis (Rochebrune, 1882)

8 Coelatura briarti (Dautzenberg, 1901)

51 Aspatharia marnoi (Jickeli, 1874)

9 Coelatura choziensis (Preston, 1910)

52 Aspatharia pfeifferiana (Bernardi, 1860)

10 Coelatura cridlandi Mandahl-Barth, 1954 11 Coelatura essoensis (Chaper, 1885) 12 Coelatura gabonensis (Ku¨ster, 1862)

53 Aspatharia rochebrunei (Jousseaume, 1886) ? A. tristis (Jousseaume, 1886) 54 Aspatharia rugifera (Dunker, 1858)

13 Coelatura hauttecoeuri (Bourguignat, 1883)

55 Aspatharia semicorrugata (Preston, 1909)

14 Coelatura horei (E.A. Smith, 1880)

56 Aspatharia subreniformis (Sowerby, 1867)

15 Coelatura hypsiprymna (von Martens, 1897)

57 Chambardia bourguignati (Bourguignat, 1885)

16 Coelatura kipopoensis (Mandahl-Barth, 1968)

58 Chambardia dautzenbergi (Haas, 1936)

17 Coelatura kunenensis (Mousson, 1887)

59 Chambardia letourneuxi Bourg. in Servain, 1890

18 Coelatura leopoldvillensis (Putzeys, 1898)

60 Chambardia moutai (Dartevelle, 1939)

19 Coelatura lobensis (Frierson, 1913)

61 Chambardia nyassaensis (Lea, 1864)

20 Coelatura luapulaensis (Preston, 1913)

62 Chambardia petersi (von Martens, 1860)

21 Coelatura mossambicensis (von Martens, 1860)

63 Chambardia rubens (Lamarck, 1819)

22 Coelatura ratidota (Charmes, 1885)

64 Chambardia trapezia (von Martens, 1897) 65 Chambardia wahlbergi (Krauss, 1848)

23 Coelatura rothschildi (Neuville & Anthony, 1906) 24 Coelatura rotula Pilsbry & Bequaert, 1927

66 Chambardia welwitschii (Morelet, 1868)

25 Coelatura stagnorum (Dautzenberg, 1890)

67 Chambardia wissmanni (von Martens, 1883)

26 Coelatura stuhlmanni (von Martens, 1897) 27 Grandidieria burtoni (Woodward, 1859)

68 Chelidonopsis hirundo (von Martens, 1881)

28 Leguminaia saulcyi (Bourguignat, 1852)

70 Mutela alata (Lea, 1864)

69 Moncetia anceyi Bourguignat, 1885

29 Mweruella mweruensis (E.A. Smith, 1908)

71 Mutela alluaudi Germain, 1909

30 Nitia acuminata (H. Adams, 1866)

72 Mutela bourguignati Bourguignat, 1885

31 Nitia chefneuxi (Neuville & Anthony, 1906)

73 Mutela dubia (Gmelin, 1791)

32 Nitia monceti (Bourguignat, 1883)

74 Mutela franci Daget, 1964

33 Nitia mutelaeformis (Germain, 1906)

75 Mutela hargeri E.A. Smith, 1908

34 Nitia teretiuscula (Philippi, 1847)

76 Mutela joubini (Germain, 1904)

35 Nyassunio nyassaensis (Lea, 1864)

77 Mutela langi Pilsbry & Bequaert, 1927

36 Nyassunio ujijiensis (Crosse, 1881)

78 Mutela legumen (Rochebrune, 1886)

37 Potomida littoralis (Cuvier, 1798)

79 Mutela mabilli (Rochebrune, 1886)

38 Prisodontopsis aviculaeformis Woodward, 1991 39 Pseudospatha tanganyicensis (E.A. Smith, 1880)

80 Mutela rostrata (Rang, 1835) 81 Mutela soleniformis Bourguignat, 1885

40 Unio abyssinicus von Martens, 1866

82 Mutela wistarmorrisi Graf & Cummings, 2006

41 Unio delphinus Spengler, 1793 42 Unio gibbus Spengler, 1793

84 Pleiodon ovatus (Swainson, 1823)

43 Unio mancus Lamarck, 1819

85 Pleiodon spekii (Woodward, 1859)

44 Unio ravoisieri Deshayes, 1848

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83 Mutela zambesiensis Mandahl-Barth, 1988

Hydrobiologia (2011) 678:17–36 Table 3 continued FAMILY ETHERIIDAE 86 Etheria elliptica Lamarck, 1807 Incertae sedis 87 Germainaia geayi (Germain, 1911) The list of species and taxonomy is as proposed by Graf & Cummings (2007a), and as modified by Araujo et al. (2009a, b, c) and Graf & Cummings (2009)

Fig. 3 Histogram of species ecoregion-occurrence. More than half of all African and Malagasy freshwater mussels occur in only one or two adjacent ecoregions. The five most widely distributed species are indicated on the graph

Fig. 4 Histogram of ecoregion richness. The five most species-rich ecoregions are indicated on the graph

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collecting localities. It is evident that overall sampling success (i.e., combining both effort and mussel presence) has been low. In principle, it would be possible to correct for this disparity in effort to make quantitative comparisons among ecoregions. For example, we could consider pseudo-absences by incorporating data on general mollusk collecting sites (Ponder et al., 2001). However, a comparable database of freshwater gastropods and veneroid bivalves is not available. We could use rarefaction curves or other resampling procedures to estimate richness based on equivalent effort (e.g., systematic quantitative sampling), but the presenceonly data of this study as well as the low apparent sampling success in many ecoregions violates the assumptions of the methods and limits the utility of their application (Heck et al., 1975; Tipper, 1979; Gotelli & Colwell, 2001; Richardson & Richards, 2008). We must simply be willing to live with the qualitative data that we have and temper our conclusions with the understanding that sampling effort has not been uniform across the freshwater ecoregions of Africa and Madagascar. We attempted to fill some holes in our museum data from the literature, but opportunities were limited given our exhaustive sampling of the vouchers on which much of the published record is based. We agree with Strayer & Dudgeon (2010) that, for the sake of time-critical conservation of freshwater biodiversity, we must assume that the qualitative patterns presented here are a sufficient estimation of freshwater mussel distributions. Despite these shortcomings, the patterns of freshwater mussel richness and endemism are valuable for determining hotspots of general aquatic diversity (Fig. 5), being significantly correlated with aquatic taxa generally (Fig. 6) and major habitat types (Fig. 7). The following discussion emphasizes the novel insights gained into unionoid biodiversity and biogeography that can now be taken into account when considering conservation priorities for the fresh waters of Africa and Madagascar. Patterns of endemism

reflect areas of concentrated sampling effort, but not necessarily high abundance. The median number of species per ecoregion is 3.5, the median number of lots is 10 (Fig. 2), and the median number of georeferenced localities is 5. The majority of ecoregions (61; 68%) are represented by fewer than ten

Areas of endemism are indicative of local evolutionary/ecological processes and valuable for identifying regionally outstanding assemblages for conservation assessments (Thieme et al., 2005). The highest species richness and the highest endemism of

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Fig. 5 Freshwater mussel species richness (a) and endemism (b) in the freshwater ecoregions of Africa and Madagascar. Ecoregions united by shared species with small ranges

(endemics occurring in only two adjacent ecoregions) are indicated by their shared outline. Distributions of endemic species are listed in Table 4

freshwater mussels are observed in the two ecoregions that comprise the White Nile catchment: Lake Victoria Basin [521] and Upper Nile [522] (Fig. 4; Table 4). This is not only a function of the high sampling effort in those areas (Fig. 2a) but is also the result of where the border between these two ecoregions has been drawn. The upper White Nile and associated Great Lakes are characterized by several species with local distributions in lakes Victoria, Albert and Edward or some combination thereof (Graf & Cummings, 2007b; Van Damme & Van Bocxlaer, 2009), though Lake Albert is currently isolated by fall-lines on the Victoria Nile and Semliki River. Lake Albert is the upper-most segment of Upper Nile [522]. The segregation of Lake Albert, with its characteristic lake-mussel fauna, from the other Great Lakes of [521] misleadingly inflates the total and endemic richness of Upper Nile [522]. Indeed, without the inclusion of the Great Lakes endemics, the freshwater mussel fauna of the upper Nile is composed of only 11 widespread species shared with the lower Nile, West Africa and/or East Africa instead of 16. This value fits well with that predicted in Fig. 6a. Alternatively, the endemic species shared between Lake Victoria Basin [521] and Upper Nile [522]

could indicate a close geographic affinity between those ecoregions—that, combined, they represent a larger biogeographical unit. Other such pairs (or triplets) of ecoregions are illustrated in Fig. 5b, and the endemic species shared between them are listed in Table 4. Analyses of the beta- and gamma-diversity of these ecoregions would contribute to an understanding of the complex histories of both the Afrotropical freshwater mussel communities and the basins that they inhabit.

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Correlation with other taxa The patterns of unionoid richness and endemism are significantly correlated with those of the fishes and other freshwater mollusks (Fig. 6). This supports the hypothesis that common evolutionary processes acted in similar ways on a taxonomically diverse assemblage of aquatic lineages. This correlation is well documented in other regions (Watters, 1992; Vaughn & Taylor, 2000). Moreover, outliers that deviate from the correlation (i.e., ecoregions where mussel richness/endemism is higher or lower than expected) suggest unique processes or violations of our initial assumptions.


27

Table 4 Ecoregion occurrences of endemic species Species

501

Unio delphinus

X

Unio gibbus

X

Margaritifera marocana Anodonta anatina

X O

Anodonta cygnea

O

Unio ravoisieri

502

503

509

511

O

O

514

515

O

O

520

521

522

523

526

530

O O X

Leguminaia saulcyi

X

Pleiodon ovatus Aspatharia droueti Coelatura essoensis

X

Nitia mutelaeformis

X

Coelatura alluaudi

X

Coelatura cridlandi

X

Coelatura hauttecoeuri

X

Nitia monceti

X

Aspatharia divaricata

X

Mutela bourguignati

X

Coelatura stuhlmanni

O

O

Nitia acuminata Chambardia trapezia

O O

O O

Mutela alluaudi

O

O

Chambardia letourneuxi

X

Unio abyssinicus

X

Nitia chefneuxi

X

1 Ecoregion endemics

3

1

1

0

0

0

1

1

6

0

1

1

1

B2 Ecoregion endemics

5

3

1

1

1

1

2

1

10

4

1

1

1

Three ecoregions stand out for their low levels of endemism. Lake Malawi [559] has lower recognized freshwater mussel richness than might be predicted given the high endemic fish diversity (Fig. 6c). The radiation of Malawi cichlid fishes (400–800 spp.) may be the product of local, rapid evolution due to sexual selection (Seehausen, 2000; Genner & Turner, 2005), and perhaps unionoid cladogenesis has not kept pace. Two ecoregions that have high freshwater gastropod endemism lack mussel endemics: Upper Congo [540] and Lower Congo Rapids [549] (Fig. 6d). The latter ecoregion is characterized by steep gradients (dropping 250 m over 380 km of river) through sandstone gorges alternating with enormous pools (Beadle, 1981; Mamonekene, 2005). This regionally unique habitat has driven the evolution of an endemic rheophilic gastropod fauna, but bivalves have been

all but excluded. The bedrock substrate is suitable only for the widespread, cementing freshwater oyster E. elliptica, and burrowing bivalves are represented by relatively few records (possibly washed down from more suitable habitats further upstream). In contrast, Upper Congo [540] has both high gastropod (34 spp.) and mussel (14 spp.) richness. However, whereas 22 species of freshwater snails are endemic to the ecoregion, most of the bivalve species are widespread in the Congo Basin. Snail richness may be somewhat inflated since eight endemics (36%) are ranked as ‘‘data deficient’’ on the Red List (Graf et al., 2011; http://www.iucnredlist.org). We do not know why the bivalves have not diversified locally to a similar extent. In Bangweulu–Mweru [544] and the permanent Maghreb of Atlantic and Mediterranean northwest

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Table 4 continued Species

533

Coelatura lobensis

X

540

542

Brazzaea anceyi

X

Coelatura horei Grandidieria burtoni

X X

Nyassunio ujijiensis

X

Pseudospatha tanganyicensis

X

Moncetia anceyi

X

Mutela soleniformis

X

Pleiodon spekii

X

Chambardia nyassaensis

544

545

549

550

551

553

555

O

Mweruella mweruensis

O

559

O O

Coelatura choziensis

X

Coelatura luapulaensis

X

Prisodontopsis aviculaeformis

X

Mutela hargeri

X

Coelatura kipopoensis

O

O

Mutela langi

X

Coelatura stagnorum

O

O

Mutela wistarmorrisi Chambardia welwitschii

X O

Chambardia moutai

O O

O

Coelatura hypsiprymna

X

Nyassunio nyassaensis

X

Mutela alata

X

1 Ecoregion endemics

1

0

8

4

0

0

1

1

0

0

3

B2 Ecoregion endemics

1

1

9

6

1

1

2

2

1

2

4

X species limited to a single ecoregion, O species occurs in two adjacent ecoregions (B2). Species are listed by geographic distribution

Africa [501–502], freshwater mussel endemism is higher than would be predicted from either the fish or other molluscan taxa (Fig. 6c, d). In the Congo Basin above and including Lake Mweru, there are four single-ecoregion endemics: Prisodontopsis aviculaeformis, Coelatura choziensis, C. luapulaensis, and Mutela hargeri. In addition, C. kipopoensis is shared only with Upper Lualaba [545], and Mweruella mweruensis is represented by a few museum records in Upper Congo [540] (Table 4). This degree of endemism is striking since both Prisodontopsis and Mweruella have been classified in their own monotypic subfamilies (Pain & Woodward, 1968). Phylogenetic data will distinguish whether these taxa are relictual lineages or if there has been rapid evolution

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within the basin (i.e., whether sister lineages occur in the same ecoregion). The observed ‘‘endemism’’ of freshwater mussels in Palearctic northwest Africa is artificial, as we did not analyze distributions in adjacent provinces (Table 4). Of the six endemic species in the permanent Maghreb [501–502], only Margaritifera marocana in Atlantic Northwest Africa [501] is restricted to Africa (Araujo et al., 2009c). The remainder of the species also inhabit the Iberian Peninsula (Araujo et al., 2009a). A single true endemic in [501–502] is consistent with the correlation with both the fishes and other mollusks (Fig. 6c, d; but see Van Damme et al., 2010, for an alternative taxonomy that would result in higher northwestern African endemism).


29

Fig. 6 Correlation of freshwater mussel richness and endemism with other taxa. Outlying ecoregions are marked with open circles and indicated by their numerical key (Table 1). a Correlation of freshwater mussel richness with fish richness (r = 0.7094, P \ 0.001). b Correlation of freshwater mussel

richness with non-unionoid mollusk richness (r = 0.5076, P \ 0.001). c Correlation of freshwater mussel endemism with fish endemism (r = 0.7064, P \ 0.001). d Correlation of freshwater mussel endemism with non-unionoid mollusk endemism (r = 0.6454, P \ 0.001)

Variation in richness among major habitat types

& Cummings, 2009), and highland rivers are characterized by fall-lines that impede upstream dispersal. There is more variation in richness among the 13 xeric ecoregions (i.e., those receiving \250 mm of precipitation annually). While the median richness is 1, Lower Nile [523] has ten species (Fig. 7). The terrestrial aspect of this ecoregion is characterized by desert habitats, but the permanent presence of the Nile makes this apparent outlier unexceptional. Though some species can persist in streams temporarily lacking surface waters (Pilsbry & Bequaert, 1927; Boss, 1974), the absence of stable fresh waters tends to lower (or extinguish) unionoid richness in xeric ecoregions with isolated catchments. This limits

Thieme et al. (2005) assigned each ecoregion to a major habitat type, among which freshwater mussel richness varies significantly (Fig. 7). Low species richness is observed among XS, HMS, and IRL. This is expected given the dependence of unionoids on ecologically stable waterways. Mussel dispersal is accomplished during their larval stage via phoresy on freshwater fishes (Watters, 1992; Graf, 1997), whereas other freshwater mollusks are capable of colonizing ephemeral or isolated habitats via avian dispersal (Rees, 1965; Cummings & Graf, 2009). Oceanic islands typically lack unionoids (but see Graf

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30


Fig. 7 Variation in freshwater mussel richness across habitats. The median richness values among the major habitat types are significantly different (Kruskal–Wallis H = 47.03, Hc = 48.28, P \ 0.001). According to Bonferroni-corrected Mann–Whitney pairwise comparisons: *Significantly different from MFR (P \ 0.05); **significantly different from SDFR (P \ 0.05). Open circles indicate outliers (1.59 interquartile

distance). Major habitat types: CBSL closed basins and small lakes; FSL floodplains, swamps and lakes; MFR moist forest rivers; MS Mediterranean systems; HMS highland and mountain streams; IRL island rivers and lakes; LL large lakes; LRD large river deltas; LRR large river rapids; SDFR savanna–dry forest rivers; SSS subterranean and spring systems; XS xeric systems

freshwater mussel distributions in the Afrotropics, given that 41% of the land area (12,362,292 km2) is classified as xeric (Thieme et al., 2005). Well-connected, permanent aquatic habitats do not guarantee the presence of freshwater mussels. For example, Tumba [538] and Mai Ndombe [547] in the central Congo Basin are devoid of mollusks, despite being surrounded by relatively mussel-rich ecoregions (Fig. 5a). These two lakes occupy the remnants of a Pliocene endorheic basin, and both have shallow, acidic, black waters with high organic and low mineral content (Beadle, 1981; Hughs & Hughs, 1992). Unionoids acquire calcium from their aqueous environment, and local concentrations of dissolved solids can limit bivalve diversity (Cummings & Graf, 2009). Beadle (1981) hypothesized that the low calcium concentration and the presence of molluscivorous fishes (e.g., Protopterus dolloi) exclude mollusks from these lakes.

Cryptic diversity

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Our analyses have revealed potential cryptic diversity in some species. For many freshwater mussels, current taxon concepts are legacies of the ‘‘lumping’’ associated with mid-twentieth century application of the Biological Species Concept (Graf, 2007). Revisionary work applying a Phylogenetic Species Concept will increase not only the quality (as judged by their suitability as terminal taxa in cladistic analyses and conservation assessments) but also the quantity of freshwater mussel species recognized from the Afrotropics (Wheeler & Meier, 2000; Agapow et al., 2004). The potential for under-estimated species richness is evident among the most widely distributed taxa (Fig. 3). For example, C. wahlbergi is widespread from South Africa through eastern Africa to the Nile Basin as well as West Africa, and five geographical


subspecies have been traditionally recognized (Mandahl-Barth, 1988; Daget, 1998). Two species, C. welwitschii and C. moutai, have recently been resurrected from this complex (Graf & Cummings, 2006b). As broadly distributed taxa with multiple allopatric segments are revised, continent-wide richness may increase. However, promotion of geographical variants to the species level will have only minor impacts on patterns of ecoregion richness and endemism since widespread ‘‘subspecies’’ tend to have large ranges ([2 ecoregions) that do not overlap. In contrast, the discovery of cryptic diversity among more localized endemics will likely increase richness and endemism in some ecoregions. For example, Coelatura hauttecoeuri in Lake Victoria Basin [521] has 12 synonyms (Daget, 1998), at least one of which (Unio ruellani Bourguignat, 1883) was recognized as valid by Haas (1969), and another (C. h. kyogae) was named as a subspecies by Mandahl-Barth (1954). Subdivision of endemic species will tend to make diversity hotspots hotter at the ecoregion scale. Accounting for cryptic diversity within C. hauttecoeuri is particularly relevant given the dire environmental situation in Lake Victoria (Witte et al., 2007; Sitoki et al., 2010), but it is not the only taxon we would identify in this context. However, taxonomic speculation is beyond the scope of our study, and the species list presented in Table 3 should not be considered definitive. Species known from few specimens Thirteen species (15%) are known from fewer than ten museum lots each: Coelatura cridlandi, C. hypsiprymna, C. lobensis, C. rothschildi, Nitia chefneuxi, Nyassunio ujijiensis, Germainaia geayi, Aspatharia divaricata, Chambardia letourneuxi, Mutela alluaudi, M. franci, M. joubini, and M. wistarmorrisi. Eleven more are each known from fewer than 20 lots. These 24 species represent 28% of the total richness for Africa and Madagascar but account for only 4% (214/5612) of georeferenced records. These taxa highlight the need for a dataset as extensive as this one and suggest that further sampling or revisionary work may reveal additional rare species. Alternatively, these rare taxa may, with further taxonomic study, be subsumed into more widespread congeners, resulting in lower richness and endemism in certain ecoregions. For the sake of symmetry, the species

31

with the largest number of records are Coelatura aegyptiaca (578 lots), Grandidieria burtoni (486), E. elliptica (454), Mutela dubia (243), and M. rostrata (212). These five species (6%) account for 35% of the total lots analyzed. Ten additional species are represented by more than 100 records each. Considerations for conservation Threats to the watersheds of Africa and Madagascar were reviewed in Thieme et al. (2005), with logging, mining, agriculture, dam and other infrastructure construction, political unrest, rapid human population growth, invasive species, and climate change among the recurrent themes (see also Seddon et al., 2011). These are general threats to fresh waters worldwide (Dudgeon et al., 2006; Strayer & Dudgeon, 2010). Our principal motivation for this study was to provide the most accurate information possible to those responsible for determining conservation priorities in the region. The utility of a species-based approach for recognizing areas of biodiversity significance has been well demonstrated (Mace, 2004), as has the need for high quality data for determining conservation goals (Darwall & Vie´, 2005). Unfortunately, conservation theory and practice has been biased toward terrestrial ecosystems despite the severe crisis facing aquatic species and habitats (Dudgeon et al., 2006; Strayer & Dudgeon, 2010), and global freshwater conservation priorities have focused primarily on freshwater fishes (Abell et al., 2008). This is despite invertebrates suffering the brunt of species declines and extinctions—especially freshwater mollusks (Lydeard et al., 2004; Strayer, 2006). Our data corroborate and expand on previous efforts to incorporate patterns of freshwater molluscan diversity into Afrotropical conservation assessments (Kristensen et al., 2009, 2010; Van Damme et al., 2010; Graf et al., 2011; Seddon et al., 2011), and we advocate a holistic approach that accounts for all freshwater taxa. Freshwater mussels in particular provide unique aesthetic and functional perspectives to the process of identifying focal species and habitats in need of management. These mollusks are interesting and charismatic, not the least for their parasitic life cycles and associated morphological and behavioral adaptations (Kat, 1984; Barnhart et al., 2008). Unionoids can be as inspirational as any other taxon used to direct the public’s attention to the importance of

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32


freshwater systems. Unionoids also perform a variety of ecosystem functions, including water filtration, nutrient cycling, biodeposition, and bioturbation of sediments, and they have a positive effect on the diversity of the benthic community overall (Vaughn & Hakenkamp, 2001; Vaughn et al., 2004, 2007; Spooner & Vaughn, 2006). Unionoids contribute to the ecological value of freshwater ecosystems and the landscapes that those ecosystems serve. Moreover, as focal species in conservation assessments, freshwater mussels provide a valuable complement to data derived from other aquatic taxa. The most recent effort to delineate the freshwater ecoregions of the world dismissed invertebrates as poor zoogeographic indicators because of their tendency for inter-basin dispersal and rapid, local speciesturnover (Abell et al., 2008). While this description may characterize aquatic insects or even some mollusks, it is hardly applicable to the Unionoida.

Compared to freshwater mussels’ sessile habit and inability to disperse across terrestrial barriers to exploit isolated habitats, it is the fishes that are the fickle transients. Freshwater mussel disjunctions are strong evidence of past confluence and are valuable complements to data from the more species-rich fishes. The patterns presented here should be taken into account when ecoregion conservation priorities are re-evaluated. Based on the conservation priorities already established, the freshwater mussels of Africa and Madagascar are in need of protection. For example, all of the freshwater ecoregions with more than one endemic freshwater mussel species (Table 4) are ranked in conservation priority class I, ‘‘… globally outstanding ecoregions that are highly threatened’’ (Thieme et al., 2005, p. 91). Of the 34 singleecoregion endemic species, 26 (76%) are known only from class I ecoregions (Fig. 8). The IUCN

Fig. 8 Endemism and Red List conservation status of freshwater mussels species among the five conservation priority classes of freshwater ecoregions established by Thieme et al. (2005). Most species occur in priority class I freshwater ecoregions, with the largest numbers of endemic, threatened, and ‘‘data deficient’’ taxa. Species conservation status is summarized in three categories: Threatened or extinct = those species ranked as Extinct, Critically Endangered, Endangered, and Vulnerable on the Red List; Stable = Near Threatened and

Least Concern species; Data Deficient = Data Deficient plus those not assessed for the Red List (Seddon et al., 2011; http://www.iucnredlist.org/). Ecoregion conservation priority classes: I globally outstanding and threatened; II continentally outstanding and threatened; III globally/continentally outstanding and intact; IV bioregionally outstanding/nationally important and threatened; V bioregionally outstanding/nationally important and intact

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recently published conservation assessments of African freshwater mussel species (Seddon et al., 2011; http://www.iucnredlist.org/), and these are summarized in Fig. 8. Class I freshwater ecoregions harbor the greatest number of threatened or extinct species. As significant is the number of taxa (35 species; 40%) that were labeled as ‘‘data deficient’’ (including 18 species for which no assessment is available). The majority of these ‘‘data-deficient’’ species occur in priority class I freshwater ecoregions (23 spp.; 66%). These criteria should be used to target specific areas where further revisionary and field research is necessary.

Conclusions The analysis of museum records described herein provides a qualitative baseline for the patterns of freshwater mussel species richness and endemism in Africa and Madagascar and underscores the value of natural history collections to biodiversity research (Suarez & Tsutsui, 2004; Pyke & Ehrlich, 2010). However, the lack of systematic sampling and the potential influence of out-dated taxonomy temper our conclusions. We do not predict that further museum work is going to fill in the lacunae in our dataset. Instead the paucity of records (or notice of absence) in many ecoregions will need to be settled with survey work in the field. Moreover, quantitative sampling is necessary to determine the current population status of taxa in all areas (e.g., Alonso & Nordin, 2003). Specimens preserved for anatomical and molecular analyses will also be a boon for phylogenetic and revisionary studies that can go beyond mere shell characters. If we want to extrapolate the future of these taxa, then we need a better understanding of both their past and their present. Given the well-documented threats to freshwater biodiversity in Africa and Madagascar, the time for this is now. Acknowledgments This research was funded by grants from the National Science Foundation to DLG (DEB-0316125, 0542575) and KSC (DEB-0316488). The authors are grateful to the curators and the collection managers who permitted access to the specimens in their charge, often hosting us for weeks. T.K. Kristensen and Michele Thieme generously provided their unpublished data on mollusk distributions in Africa. Tim Hayes, Katie Vazquez, Jerry Graf, Jeremy

33 Tiemann, and Jonah White assisted with specimen image processing and georeferencing. Bert Van Bocxlaer and an anonymous reviewer provided many useful suggestions and comments that improved this article. The authors express their thanks to all those mentioned above.

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