Cage Aquaculture And Environment In Lake Malawi: An Assessment Of Water .

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Cage aquaculture and environment in Lake Malawi: anassessment of water quality, food web shifts, anddevelopment of a decision support tool for sustainableaquacultureA DISSERTATIONSUBMITTED TO THE FACULTY OF THE GRADUATE SCHOOLOF THE UNIVERSITY OF MINNESOTAByMessias Alfredo MacuianeIN PARTIAL FULFILMENT OF THE REQUIREMENTSFOR THE DEGREE OFDOCTOR OF PHILOSOPHYAdvisors: Professors: Robert E Hecky and Stephanie GuildfordApril, 2014

Messias Alfredo Macuiane 2014

iAcknowledgementsSpecial thanks go to Drs: Robert E. Hecky and Stephanie J. Guildford forworking with me over the past four and half years as my advisors and sponsors atUniversity of Minnesota Duluth (UMD), without them my journey wouldn’t have beenpossible. I enjoyed having their support, guidance in all stages of my research project.I thank Drs. Raymond Newman, Jay Austin, and Thomas Hrabik for serving asacademic committee members. I sincerely thank the WorldFish Center for providingpartial support during my first academic year. Dr. António Hoguane from EduardMondlane University/Mozambique played a major role in getting me started atWorldFish Center. I thank Dr. Daniel Jamu, former Regional Director for SouthernAfrica at WorldFish Center and now Aquaculture Specialist at Maldeco Aquaculture forhis support towards my PhD. Professor Randall Hicks from Department of Biology/UMDplayed an important role in sourcing additions financial support during the period whenmy professors were retired and away from Duluth.I would like to thank the Department of Fisheries for supporting my Masters andDoctorate research in Malawi and for providing accommodation and laboratory facility atMalawi College of Fisheries. I am grateful to Maldeco Aquaculture Limited for allowingme to conduct field research in their farm. The staff members provided transportation andsupport during data collection at the farm.Funding was provided by the Office of International Programs-GlobalSpotlight/University of Minnesota and New Partnership for African Development(NEPAD). I thank Dr Emmanuel Kaunda from University of Malawi and Dr. SloansChimatiro from NEPAD for providing additional support for field research activities andtravel to Malawi through Funding through the NEPAD Regional Fish Node-SANBio.Many thanks to Ms Kathy Oliver, Yvonne Chan, Sarah Grosshuesch, and allmembers of Large Lakes Observatory for providing valuable guidance. My colleagues,Geoffrey House, Thomas Pevan, Rozhan Zakaria, Jillian Votava, Hongyu Li, Jilying Li,and Lucas Gloege contributed greatly in many aspects of my career at UMD. I would liketo thank Bonnie Anderson from University of Minnesota Twin Cities for guiding me inacademic issues during my first two years in Duluth.

iiDedicationTo my wife Rosita, my daughter Claire Cátia Macuiane and son Messias AlfredoMacuiane Junior, my nephews, my mother Catarina Gilberto Macuiane, my brothers andsisters, thank you for your endless support.

iiiAbstractThe impact of cage aquaculture on the water quality and native fish communitywas studied between November 2011 and September 2012 in the South East Arm of LakeMalawi. This ancient African Great Lake has the greatest number of fish species of anylake in the world, and the fishery is a major source of animal protein in Malawi.However, the decline of the capture fishery stocks has forced the Government of Malawito promote cage aquaculture. The Maldeco Aquaculture Limited is the first cageaquaculture operation initiated in 2004 to farm endemic and native fish species in LakeMalawi at commercial scale. Unfortunately there is no legal framework for sustainablecage aquaculture development. The study found that cage aquaculture attracts wild fishpopulations and also changes their community structure. However, the diversity was notsignificantly affected by the cage farm despite the increased abundance of fish, especiallysmaller fish. Water temperature and dissolved oxygen were minimal between April andJune, a period that cage aquaculture farms should consider as critical in their operation.Chlorophyll a had a single seasonal peak in April concurrent with the minimum intransparency. There was no significant difference in water quality parameters between theaquaculture site and sites 5 km away. Stable isotope signatures of carbon (δ13C) andnitrogen (δ15N) of the wild fish revealed shifts in small particle feeding planktivorous fishand possibly in zooplanktivorous fish, but not in benthivorous, molluscivorous, andzoobenthivorous fishes which maintained their natural diets even at the farm site. Adissolved oxygen model indicated that the average carrying capacity of the farm is1,870,000 96, kg. A mean stocking density of 23,000 440kg per cage is recommendedto allow adequate fish growth rates and attainment of desirable marketable size within a

ivshort cycle without significant impact on oxygen concentration. Un-regulated expansionof cage aquaculture activities at Maldeco Aquaculture farm or increase in the number ofcage farms has the potential of increasing changes in wild fish community structure,modifying food webs, and causing conflicts with local fishermen.

vTable of ContentsList of Figures . xiChapter 1 Overview of the fisheries sector in Malawi. 11.1 Introduction . 11.2 Thesis objectives and hypothesis . 4Chapter 2 Changes in fish community structure associated with cage aquaculture in Lake Malawi. 62.1 Introduction . 82.2 Materials and methods . 122.2.1 Lake Malawi. 122.2.2 Study area . 132.2.3 Sample collection . 152.2.4 Data analysis . 172.3 Results . 192.3.1 Changes in fish community structure . 272.3.2 Fish abundance, biomass, and diversity indices . 342.3.3 Health status of fishing sites . 362.3.4 Diversity indices. 392.5 Discussion . 402.4.1 Implications to fisheries and aquaculture policy . 442.5 Conclusion . 462.7 Recommendations . 48Chapter 3 Temporal and spatial changes in water quality parameters in Lake Malawi/Niassa,Africa: implications for cage aquaculture management. 513.1 Introduction . 533.2 Materials and methods . 573.2.1 Data collection . 573.2.2 Statistical methods . 603.3 Results . 623.4 Discussion . 683.5 Conclusions . 79

viChapter 4 Application of δ13C and δ15N isotopes to trace the use of cage aquaculture wastes bywild fish populations in Lake Malawi, Africa . 814.1 Introduction . 834.2 Materials and methods . 924.2.1 Sampling procedure . 924.3 Results and discussion . 954.3.1 Commercial feed . 954.3.2 Farmed fish . 974.3.3 Cage aquaculture and wild fish populations . 994.3.4 Trophic interactions among wild fish populations. 1104.4 Conclusion . 113Chapter 5 Oxygen consumption rates of Oreochromis karongae (Trewavas, 1941) andOreochromis shiranus (Boulanger, 1896) . 1155.1 Introduction . 1165.2 Materials and methods . 1185.3 Results and discussion . 120Chapter 6 Assessing the impact of a tilapia cage aquaculture farm and development of a carryingcapacity model for sustainable cage aquaculture in Lake Malawi . 1266.1 Introduction . 1286.1.1 Carrying capacity models . 1316.2 Materials and methods . 1356.2.1 Study area . 1356.2.2 Sampling procedure . 1376.2.3 The sub-model of water quality in fish cages . 1406.2.4 Data analysis . 1426.3 Results . 1446.3.1 Spatial and temporal changes in dissolved oxygen concentrations at the farm perimeter. 1446.3.2 Carrying capacity estimates based on perimeter observations . 1586.3.3 Cage effect and cage based carrying capacity estimates. 1616.4 Discussion . 1816.4.1 Farm perimeter observations and carrying capacity. 1816.4.2 Model application and recommendations . 1856.5 Conclusion . 189

viiChapter 7 Thesis conclusions. 191Bibliography . 195

viiiList of TablesTable 2- 1 Fish species and numbers in parentheses caught in February 2012. . 23Table 2- 2 Fish species and numbers in parentheses caught in April 2012. . 24Table 2- 3 Fish species and numbers in parentheses caught in June 2012. . 25Table 2- 4 Fish species and numbers caught in parentheses in August 2012. . 26Table 2-5 SIMPER analysis for fish community structure between fishing sites 1 and 2, withdissimilarity cut-off set at 50% cumulative contribution. Mean abundance (square rooted data)expressed as individuals per site. . 30Table 2- 6 SIMPER analysis for fish community structure between fishing sites 2 and 3, withdissimilarity cut-off set at 50% cumulative contribution. Abundance (square rooted data)expressed as individuals per site. . 31Table 2- 7 SIMPER analysis for fish community structure between February and April, withdissimilarity cut-off set at 50% cumulative contribution. Abundance (square rooted data)expressed as individuals per site. . 32Table 2- 8 SIMPER analysis for fish community structure between February and June, withdissimilarity cut-off set at 50% cumulative contribution. Abundance (square rooted data)expressed as individuals per site. . 33Table 2- 9 SIMPER analysis for fish community structure between June and August, withdissimilarity cut-off set at 50% cumulative contribution. Abundance (square rooted data)expressed as individuals per site. . 34Table 2-10 One-Way ANOVA of fish abundance, biomass, number of fish species, diversityindices, and W-statistic bvalues at fishing sites. . 35Table 3- 1 Geographical location of sampling sites and their replicates (ST-1,1 is site 1 replicate1, ST-1,2 is site 1 replicate 2, ST-2,1 is site 2 replicate 1, ST-2,2 is site 2 replicate 2, ST-3,1 issite 3 replicate 1, and ST-3,2 is site 3 replicate 2), depth of the water at the site, distance to thefarm, and distance to shore line. The coordinated (longitude and latitude) are presented inUniversal Transverse Mercator (UTM) system. . 59Table 4- 1 Mean ( SE) δ13C and δ15N of commercial feeds used at the aquaculture farm duringthis study. SE standard error. Results are compared with those of Gondwe et al (2012) for thesame farm. The feed is milled locally from imported fish meal and local grains. . 96Table 4- 2 Mean ( SE) δ13C and δ15N of caged fish and their mean total weight. . 98Table 4- 3 Mean ( SE) δ13C and δ15N of wild fish populations from fishing sites 1, 2, and 3. . 105Table 5- 1 Oxygen consumption rates of O. karongae and O. shiranus from 14 experimentsconducted in February, April, June, and August 2012 at Maldeco Aquaculture Farm. Onlyexperiments with a linear portion of change in DO for at least an hour was used to estimate theOCR. [O2] to is the initial dissolved oxygen concentration, is the O2] t1 final dissolved oxygenconcentration at the end of the experiment. . 123

ixTable 6- 1 One-way ANOVA for spatial (between sites) and temporal (day and night) data foraverage DO between 0 and 1 m extracted from the profiles between November 2011 andSeptember 2012. . 156Table 6- 2 Carrying capacity estimates of Maldeco aquaculture farm between December 2011 andSeptember. 2012. O2IN is DO flowing in and O2OUT DO flowing out of the farm, O2MIN is theminimum DO, Ui(t) is current in and Uo(t) is current flowing outside the farm, UMIN is minimumcurrents, PF is permeability of the farm, LF is length of the farm. OCR is the specific oxygenconsumption of fish, OX1 is oxygen consumption of fish at the farm, and CC is the carryingcapacity of the farm. . 170Table 6- 3 Carrying capacity estimates of individual cage in December 2012. O2IN/O2OUT is theDO flowing out of the cage, O2MIN is the minimum DO, Ui(t) is the current in and Uo(t) is thecurrent flowing outside the cage, UMIN is minimum currents, Pc is permeability of the cage, LC islength of the cage. OCR is the specific oxygen consumption of fish, OX1 is oxygen consumptioninside the cage, and CC is the carrying capacity of the farm. . 171Table 6- 4 Carrying capacity estimates of individual cage in January 2012. . O2IN is the DOflowing in and O2OUT is the DO flowing out of the cage, O2MIN is the minimum DO, Ui(t) is thecurrent in and Uo(t) is the current flowing outside the cage, UMIN is minimum currents, Pc ispermeability of the cage, LC is length of the cage. OCR is the specific oxygen consumption offish, OX1 is oxygen consumption inside the cage, and CC is the carrying capacity of the farm. 172Table 6- 5 Carrying capacity estimates of individual cage in February 2012. O2IN is the DOflowing in and O2OUT is the DO flowing out of the cage, O2MIN is the minimum DO, Ui(t) is thecurrent in and Uo(t) is the current flowing outside the cage, UMIN is minimum currents, Pc ispermeability of the cage, LC is length of the cage. OCR is the specific oxygen consumption offish, OX1 is oxygen consumption inside the cage, and CC is the carrying capacity of the farm. 173Table 6- 6 Carrying capacity estimates of individual cage in March 2012. O2IN is the DO flowingin and O2OUT is the DO flowing out of the cage, O2MIN is the minimum DO, Ui(t) is the current inand Uo(t) is the current flowing outside the cage, UMIN is minimum currents, Pc is permeability ofthe cage, LC is length of the cage. OCR is the specific oxygen consumption of fish, OX1 isoxygen consumption inside the cage, and CC is the carrying capacity of the farm. 174Table 6- 7 Carrying capacity estimates of individual cage in April 2012. O2IN is the DO flowing inand O2OUT is the DO flowing out of the cage, O2MIN is the minimum DO, Ui(t) is the current in andUo(t) is the current flowing outside the cage, UMIN is minimum currents, Pc is permeability of thecage, LC is length of the cage. OCR is the specific oxygen consumption of fish, OX1 is oxygenconsumption inside the cage, and CC is the carrying capacity of the farm. . 175

xTable 6- 8 Carrying capacity estimates of individual cage in May 2012. O2IN is the DO flowing inand O2OUT is the DO flowing out of the cage, O2MIN is the minimum DO, Ui(t) is the current in andUo(t) is the current flowing outside the cage, UMIN is minimum currents, Pc is permeability of thecage, LC is length of the cage. OCR is the specific oxygen consumption of fish, OX1 is oxygenconsumption inside the cage, and CC is the carrying capacity of the farm. . 176Table 6- 9 Carrying capacity estimates of individual cage in June 2012. O2IN is the DO flowing inand O2OUT is the DO flowing out of the cage, O2MIN is the minimum DO, Ui(t) is the current in andUo(t) is the current flowing outside the cage, UMIN is minimum currents, Pc is permeability of thecage, LC is length of the cage. OCR is the specific oxygen consumption of fish, OX1 is oxygenconsumption inside the cage, and CC is the carrying capacity of the farm. . 177Table 6- 10 Carrying capacity estimates of individual cage in July 2012. O2IN is the DO flowingin and O2OUT is the DO flowing out of the cage, O2MIN is the minimum DO, Ui(t) is the current inand Uo(t) is the current flowing outside the cage, UMIN is minimum currents, Pc is permeability ofthe cage, LC is length of the cage. OCR is the specific oxygen consumption of fish, OX1 isoxygen consumption inside the cage, and CC is the carrying capacity of the farm. 178Table 6- 11 Carrying capacity estimates of individual cage in August 2012. O2IN is the DOflowing in and O2OUT is the DO flowing out of the cage, O2MIN is the minimum DO, Ui(t) is thecurrent in and Uo(t) is the current flowing outside the cage, UMIN is minimum currents, Pc ispermeability of the cage, LC is length of the cage. OCR is the specific oxygen consumption offish, OX1 is oxygen consumption inside the cage, and CC is the carrying capacity of the farm. 179Table 6- 12 Carrying capacity estimates of individual cage in September 2012. O2IN is the DOflowing in and O2OUT is the DO flowing out of the cage, O2MIN is the minimum DO, Ui(t) is thecurrent in and Uo(t) is the current flowing outside the cage, UMIN is minimum currents, Pc ispermeability of the cage, LC is length of the cage. OCR is the specific oxygen consumption offish, OX1 is oxygen consumption inside the cage, and CC is the carrying capacity of the farm. 180

xiList of FiguresFigure 2-1 Lake Malawi (left) and fishing sites (ST-1,1 is fishing site 1 replicate 1, ST-1,2 isfishing site 1 replicate 2, ST-2,1 is fishing site 2 replicate 1, ST-2,2 is fishing site 2 replicate 2,ST-3,1 is fishing site 3 replicate 1, and ST-3,2 is fishing site 3 replicate 2) including MaldecoAquaculture farm (right). . 16Figure 2-2 Dendrogram of similarity of sampling site replicates based on square roottransformation of abundance of fish species using Bray-Curtis similarity index. . 27Figure 2-3 Non-metric multi-dimensional scaling (NMDS) plot of spatial and temporal anddistribution of fish community structure. Symbols represent sites, open circles represent site 1,black circles represent site 2, and the x represent site 3. . 28Figure 2-4 a) Average number of fish species, b) average fish biomass, c) average fish abundance,d) and average W-statistics value recorded at fishing sites 1, 2, and 3 in February, April, June, andAugust 2012. . 36Figure 2- 5 Abundance Biomass Curves (ABC) curves for fish community in Lake Malawi.Abundance ( ); biomass ( ). . 38Figure 2-6 a) Average Pielou’s Evenness diversity index, b) average Simpson diversity index, c)average Shannon diversity index, and d) average Margalef diversity index from fish samplings atfishing sites 1, 2, and 3 in February, April, June, and August 2012. . 39Figure 2-7 Abundance-rank of fish communities recorded at fishing sites 1, 2, and 3 in February,April, June, and August 2012. . 44Figure 2-8 Local fishermen fishing inside Maldeco Aquaculture Limited Farm in 2012. . 50Figure 3- 1 Lake Malawi (left) and sampling sites (ST-1,1 is site 1 replicate 1, ST-1,2 is site 1replicate 2, ST-2,1 is site 2 replicate 1, ST-2,2 is site 2 replicate 2, ST-3,1 is site 3 replicate 1, andST-3,2 is site 3 replicate 2) including Maldeco Aquaculture farm (right) . 60Figure 3- 2 Temporal (month) and spatial (site) changes in surface water quality parameters inLake Malawi along a north-south 10 km transect including the tilapia cage aquaculture farm. 67Figure 3- 3 CTD chlorophyll a profiles at sampling sites in February: a), b), and c); April: d), e);f); June: g), h), and i); August: j), k), and l). Red dot is replicate 1 and blue dot is replicate 2. . 78Figure 4- 1 Lake Malawi and the fishing sites in the southeast arm: site 1 replicate 1 (11), site 1replicate 2 (12), site 2 (aquaculture farm) replicate 1 (21), site 2 replicate 2 (22), site 3 replicate 1(31), and site 3 replicate 2 (32). . 94Figure 4- 2 Mean δ13C ( SE) and δ15N ( SE) of commercial feeds fed to caged fish duringproduction cycle. Mean δ13C ( SE) and δ15N ( SE) of commercial feeds sampled by Gondwe etal. (2012) are included. . 96

xiiFigure 4- 3 Mean δ13C ( SE) and δ15N ( SE) of commercial feeds and cages fish sampled inFebruary and April. Mean δ13C ( SE) and δ15N ( SE) of commercial feeds and caged fishmeasured by Gondwe et al. (2012) are included. . 99Figure 4- 4 Mean stable isotopes (δ13C and δ15N) of caged fish and planktivorous fish sampled inFebruary, April, June, and August 2012 at fishing site 1 (ST1), fishing site 2 (ST2), and fishingsite 3 (ST3). Mean (δ13C and δ15N) of caged fish measured by Gondwe et al. 2012 are included. 106Figure 4- 5 Mean stable isotopes (δ13C and δ15N) of caged fish and benthivorous fish sampled inFebruary, April, June, and August 2012 at fishing site 1 (ST1), fishing site 2 (ST2), and fishingsite 3 (ST3). Mean (δ13C and δ15N) of caged fish measured by Gondwe et al. 2012 are included. 107Figure 4- 6 Mean stable isotopes (δ13C and δ15N) of caged fish and molluscivorous fish sampledin February, April, June, and August 2012 at fishing site 1 (ST1), fishing site 2 (ST2), and fishingsite 3 (ST3). Mean (δ13C and δ15N) of caged fish measured by Gondwe et al. 2012 are included. 108Figure 4- 7 Mean stable isotopes (δ13C and δ15N) of caged fish and zoobenthivorous fish sampledin February, April, June, and August 2012 at fishing site 1 (ST1), fishing site 2 (ST2), and fishingsite 3 (ST3). Mean (δ13C and δ15N) of caged fish measured by Gondwe et al. 2012 are included. 109Figure 4- 8 Mean stable isotopes (δ13C and δ15N) of caged fish and zooplanktivorous fish sampledin February, April, June, and August 2012 at fishing site 1 (ST1), fishing site 2 (ST2), and fishingsite 3 (ST3). Mean (δ13C and δ15N) of caged fish measured by Gondwe et al. 2012 are included. 110Figure 4- 9 Average body weight of farmed fish in cages 45 and 46 harvested in February andApril 2012 respectively at Maldeco Aquaculture farm. . 112Figure 5- 1 Change in dissolved oxygen concentration in the respirometer oxygen consumptionby O. shiranus and O. karongae in the respirometer. . 121Figure 5- 2 Oxygen consumption rates and weight relationship of O. shiranus and O. karongae. 125Figure 6- 1 Map of the location of Lake Malawi and location of Maldeco Aquaculture Farm (rightpanel) sh

Malawi. This ancient African Great Lake has the greatest number of fish species of any lake in the world, and the fishery is a major source of animal protein in Malawi. However, the decline of the capture fishery stocks has forced the Government of Malawi to promote cage aquaculture. The Maldeco Aquaculture Limited is the first cage aquaculture .

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