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THE ECOLOGICAL EFFECTS OF Undaria pinnatifida:

A Critical Assessment and Summary of the Literature

6 May 1999

Paul R Dean. BSc, Dip Sci, MSc (Dist).

In todays world, Scientific advice is often used to make decisions that have strong and wide ranging repercussions. If this advice is poor or inaccurate the results of the decisions can be costly. While writing my masters thesis on the eco-physiology of the seaweed Undaria pinnatifida (Harvey) Suringar, I encountered many articles on the ecological effects of the introduction of this seaweed. Many of the conclusions of these articles were contradictory. This report is my endeavour to sort out the facts and provide a basis for a scientific assessment.

The Ecological Effects of Undaria pinnatifidaDraft Jan 00

INTRODUCTION

Over the last decade a number of studies and reports on the ecological effects of the introduced seaweed Undaria pinnatifida and surveys of U. pinnatifida that make statements about it’s ecological effects have been conducted. Many of these reports and surveys derive conclusions that are different and opposing to each other. This makes it difficult to quickly assess what the true ecological effects of U. pinnatifida are. To my knowledge no one has examined the findings of all these reports and scrutinised the scientific methods used, or for literature surveys the accuracy and range of references examined. This is the objective of this report.

Twenty articles making statements on the ecological effects of Undaria pinnatifida dated up until May 1998 were found (Table 1). It is the information provided by these that I am critically assessing so that a scientifically valid picture of the ecological effects of U. pinnatifida may be attained. Of the twenty articles making statements about the ecological effects, four were pure literature searches with no fieldwork or experimental component. Fourteen had some form of biological survey work (usually performed by SCUBA) ranging from very minor surveys to compliment a literature search, to large scale surveys of U. pinnatifida distribution, with none of the surveys having any experimental component. The remaining two articles had experimental work examining the ecological effects of U. pinnatifida.

The main body of this report is divided into 3 sections. The 1st section briefly explains the basic attributes, as determined by prominent ecologists, that an ecological study on competitive interactions must possess to be of scientific value. The 2nd section is large, and progresses through all twenty articles, examining the findings and opinions contained within the articles, and critically assessing the articles validity in respect of the methods used and the attributes discussed in section 1. The 3rd and final section combines the results from section 2 and provides an assessment of Undaria pinnatifida’s ecological impact based on these results and further scientific literature.

Table 1. Articles examined.

Houghton, C., Lawrence, B., Lettink, M., Numata, M. 1997: Environmental impact assessment: ecological and economic impacts of Undaria pinnatifida in New Zealand. Project for Diploma in Wildlife Management, Zoology Department, University of Otago, New Zealand. / Lit
Parsons, M J. 1995: Status of the introduced brown seaweed Undaria in New Zealand. Conservation Advisory Science Notes No 112. Department of Conservation, Wellington, New Zealand. / Lit
Rueness, J. 1989: Sargassum muticum and other introduced Japanese macroalgae: Biological pollution of European coasts. Marine Pollution Bulletin Vol 20, no 4: 173-176 / Lit
Walker, DI., Kendrick, G A. 1998: Threats to macroalgal diversity: marine habitat destruction and fragmentation, pollution and introduced species. Botanica Marina 41: 105-112 / Lit
Battershill, C., Miller, K., and Cole, R. 1998: The understorey of marine invasions. Seafood New Zealand, March 1998, pp 31-33 / Sur
Brown, M T. and Lamare, M D. 1994: The distribution of Undaria pinnatifida (Harvey) Suringer within Timaru Harbour, New Zealand. Japanese Journal of Phycology 42: 63-70 / Sur
Casas, G N. and Piriz, M L. 1996: Surveys of Undaria pinnatifida (Laminariales, Phaeophyta) in Golfo Nuevo, Argentina. Hydrobiologia 326/327: 213-215 / Sur
Castric-Fey, A., Girard, A., and L’Hardy-Halos, M Th. 1993: The distribution of Undaria pinnatifida (Phaeophyceae, Laminariales) on the coast of St Malo (Brittany, France). Botanica Marina 36: 351-358 / Sur
Fletcher, R L., Manfredi, C. 1995: The occurrence of Undaria pinnatifida (Phaeophyceae, Laminariales) on the south coast of England. Botanica Marina 38: 355-358 / Sur
Floc’h, J Y., Pajot, R., and Wallentinus, I. 1991: The Japanese brown alga Undaria pinnatifida on the coast of France and its possible establishment in European waters. Journal du Conseil. Conseil International Pour l’Eploration de la Mer. 47: 379-390 / Sur
Hay, C H. 1990: The dispersal of sporophytes of Undaria pinnatifida by coastal shipping in New Zealand, and implications for further dispersal of Undaria in France. British Phycological Journal 25: 301-313 / Sur
Hay, C H. 1990/1991: Ecological implications of the adventive kelp Undaria pinnatifida. DOC Science Project Summaries 1990/1991. Conservation Estate Management and Advocacy, Science, and Research Internal Report No 119, pgs 11-12 / Sur
Hay, C H. and Luckens, P A. 1987: The Asian kelp Undaria pinnatifida (Phaeophyta: Laminariales) found in a New Zealand harbour. New Zealand Journal of Botany 25: 329-332 / Sur
Hay, C H. and Villouta, E. 1993: Seasonality of the adventive Asian kelp Undaria pinnatifida in New Zealand. Botanica Marina 36: 461-476 / Sur
Miller, K., Cole, R., and Battershill, C. 1997: Marine invasions: the spread of the introduced Asian alga, Undaria, in New Zealand waters. Water & Atmosphere 5(2): 8-9 / Sur
Sanderson, J C. 1990: A preliminary survey of the distribution of the introduced macroalga, Undaria pinnatifida (Harvey) Suringer on the east coast of Tasmania, Australia. Botanica Marina 33: 153-157 / Sur
Sanderson, J C. and Barrett, N. 1989: A survey of the distribution of the introduced japanese macroalga Undaria pinnatifida (Harvey) Suringer in Tasmania, December 1988. Department of Sea Fisheries, Tasmania, Australia, Technical Report 38 / Sur
Stuart, M D. 1997: The seasonal ecophysiology of Undaria pinnatifida (Harvey) Suringar in Otago Harbour, New Zealand. PhD thesis, University of Otago, Dunedin, New Zealand. / Sur
Floc’h, J Y., Pajot, R., and Mouret, V. 1996: Undaria pinnatifida (Laminariales, Phaeophyta) 12 years after its introduction into the Atlantic Ocean. Hydrobiologia 326/327: 217-222 / Exp
Russell, L. 1997: Community ecology and nutrient ecophysiology of Undaria pinnatifida (Harvey Suringar) in OtagoHarbour. BSc (Hons) dissertation, University of Otago, Dunedin, New Zealand. / Exp

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The Ecological Effects of Undaria pinnatifidaDraft Jan 00

SECTION 1. EXPERIMENTAL DESIGN

To attain scientifically valid data on competitive interactions well designed manipulative experiments must be carried out (Connell 1975, Underwood and Denley 1984, Wiens 1984). These experiments must be manipulative and not “natural experiments” (Underwood 1986). There is general agreement among ecologists that “natural experiments” are of little or no value in examining processes such as competition, as the nature of these studies makes it likely that non-competitive interactions are the cause of the differences observed (Underwood 1986). “Natural experiments” are studies where an area where a supposed competitor is naturally absent is compared to an area where the supposed competitor is present, and conclusions drawn from the differences observed.

The type of measurements made of the experimental sites to quantify the effects of competition also affect the validity of the data. Schiel and Foster (1986) conclude that questions concerning the recruitment and longevity of a species and change in size composition of algal communities can only be addressed by enumerating individuals. I.e. the number of individuals in the study site has to be assessed; standing crop measurements e.g. biomass and percent cover estimates can not be used for any consideration of the population biology or demography of algal species and therefore have little use in assessing interactions (Schiel and Foster 1986).

The commonest method used to detect the effects of one algal species on another is the removal of canopies, with observations on the subsequent recruitment of each species (Schiel 1990). This manipulative experiment mimics the natural clearances by storms or grazing. The enumeration of individuals is highly important in these canopy clearance experiments as it would otherwise be unclear whether new recruitment has occurred or if small juveniles already present have grown to replace the canopy (Schiel and Foster 1986).

Replication and controls are also important factors in the design of a valid experiment (Kingsford 1998). This is especially important where dealing with seaweeds, as seaweed stands show great natural variation both spatially and temporally (Choat and Schiel 1982, Dayton 1985, Schiel and Foster 1986, Schiel 1988, Foster 1990).

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The Ecological Effects of Undaria pinnatifidaDraft Jan 00

SECTION 2. SUMMARIES OF PREVIOUS WORK

LITERATURE SURVEYS

The use of information from pure literature searches must be used with caution. The validity of the conclusions in literature searches must be assessed by examining the variety, quality, and number of references used to back up their conclusions and the accuracy with which statements from these references have been reported. Unfortunately literature searches can not provide any new basic facts about the topic examined, but can identify areas where there appear to be contradicting results and further research is needed. The findings of the four literature surveys along with a critical assessment of the articles follows.

Houghton et al. (1997)

In their Environmental Impact Assessment report, Houghton et al. (1997) concluded that Undaria pinnatifida had many characteristics of an invasive species and would dramatically alter the marine ecosystem having a predominantly negative effect. They also state that Undaria has a window from May - September in which it may recruit into disturbed patches while other large brown seaweeds can not. A check of this article shows that it is of extremely poor quality. Containing a number of erroneous references to back up the conclusions in which the referred to articles do not support the statements of Houghton et al. (1997) or do not even cover the subject being discussed.

These erroneous references are: Pg 7 “Colonisation is extremely aggressive in high disturbance and erosion prone areas (Miller et al. 1997)”, Miller et al. (1997) does not suggest this; Pg 11, Figure 4 of Houghton et al. (1997) is attributed to be after the data presented in Hay and Villouta (1993), but the length representation shown does not at all follow the seasonal changes found in Wellington, Timaru, or Oamaru by Hay and Villouta (1993); Pg 22 “Undaria is able to colonise disturbed areas (McShane et al. 1996)”, the article McShane et al. (1996) does not even mention Undaria; Pg 24 “Indigenous fauna potentially affected include chitons, limpets, snails, and small molluscan grazers in cobbled areas (Creese 1988)”, Creese (1988) does not say these invertebrates are potentially affected, Houghton et al. (1997) suggest this.

Houghton et al. (1997) also state, without reference, that paua settle in “coralline barrens” and that Undaria invades coralline barrens, hence will lessen the settlement of paua. This is in complete contrast to the experimental literature discussed later in section 3. The presentation of conclusions from the articles in the bibliography appeared to be highly biased. Six of the articles examined by the authors concluded that Undaria would not have detrimental environmental effects; Hay 1990/1991, Floc’h et al. 1991, Hay and Villouta 1993, Brown and Lamare 1994, Parsons 1995, Floc’h et al. 1996. Of these six only one was reported in the text, Brown and Lamare (1994). Houghton et al. (1997) stated that the conclusions reached by Brown and Lamare (1994) were incorrect. From communication with the authors it was found that the report was part of the course work for a 4th year Diploma Course and that the authors did not have a Marine botany or Marine ecology background.

Parsons (1995)

The conclusions reached by the Department of Conservation report Parsons (1995) were:

  • Undaria will become part of the natural community of marine organisms, and will not displace any other species completely.
  • Since the initial introduction of the sporophyte, plants of Undaria have become part of the natural community of algae and marine animals in nearby habitats, successfully maintaining themselves without excluding any particular native species.
  • Although Undaria will compete for space with the algae in this community it does not to date seem to have occupied any natural communities to the exclusion of other species.
  • Undaria plants are more fragile than tough native brown algal species such as Carpophyllum. Suggesting that Undaria would not readily grow in the conditions favoured by Carpophyllum.
  • Drift is not likely to be a factor in the spread of Undaria in New Zealand.

The DoC report by Parsons (1995) was a large scale survey with 27 cited references and 40 additional references in a separate bibliography. A check of all references found no misquotation of references. The conclusions of the report were supported by and based on correctly quoted references.

Rueness (1989)

Rueness (1989) only mentions Undaria briefly (2 paragraphs) and says that Undaria may be potentially harmful. The four references used were all correctly quoted.

Walker and Kendrick (1998)

Walker and Kendrick (1998) in their section on Undaria suggests that there is a high probability of Undaria colonising the temperate shores of Australia, and there may be a resulting change in community structure and food webs as a result. The section in Walker and Kendrick (1998) on Undaria is of a low standard. The other sections in Walker and Kendrick (1998) were not critically assessed and have not been commented on.

The major problem was misquotation, where possibilities talked about by the authors Walker and Kendrick (1998) reference are presented as scientific fact by Walker and Kendrick (1998): Pg 108 “Once established it has proven impossible to eradicate (Hay 1990, Sanderson 1990)”, Hay (1990) and Sanderson (1990) do not report on any attempts to eradicate Undaria as attempts to eradicate Undaria have only occurred from 1997 onwards; Pg 108 “Undaria grows faster than the grazing rates of the urchins (Sanderson and Barrett 1989)”, Sanderson and Barrett (1989) state that one reason Undariamay be plentiful is that it may grow faster that the grazing rates of the urchins, although no experiments have been performed to examine this. This section on Undaria in Walker and Kendrick (1998) appears to be based on a very small literature survey (total of 6 references) with 2/3 rds of citations coming from Sanderson and Barrett (1989).

BIOLOGICAL SURVEYS

Biological surveys are able to provide us with a range of facts about an organism, i.e. where it is found, the conditions that it has been found in, and how many there are. But can not tell us why they are found where they are or about their interactions with other organisms. The findings of the fourteen surveys, the opinions of the authors, and a critical assessment of the articles follows.

Battershill et al. (1998)

Battershill et al. (1988) suggests that Undaria is displacing Carpophyllum spp’s from a rocky edge of WellingtonHarbour. Also suggested is that the sub canopy is substantially changed by the presence of Undaria. This is based on the examinations of five 1 m2 quadrates in three densities of Undaria at two sites

Battershill et al. (1998) is a small-scale semi quantitative survey of the distribution of Undaria and other marine species in WellingtonHarbour and the Marlborough Sounds. This study is a classic example of a “natural experiment”. The authors must have recognised this and have included a one-sentence caveat in their article explaining that nothing can be shown by a study of this design. Their “evidence” for Undaria displacing Carpophyllum is that there are separate patches of Undaria and Carpophyllum and that the denser the Undaria the less Carpophyllum is found, and visa-versa. The densities in this study were not measured but were only estimated by those in the field (R Cole pers. com.).

The use of % cover when examining the algal abundance is another serious mistake in this study, as the actual no of individuals should have been used, as explained in section one. Many of the changes to the sub canopy species that Battershill et al. (1998) say occur in WellingtonHarbour are not evident from their figures. Figure 3, pg 33 does not show a significant change (=0.05) in the % cover of Lithothamnion or encrusting coralline algae in December or in March from outside to inside of patches. The % cover of turfing algal species also does not show a significant change (=0.05) from outside to inside or low to dense in December, or from outside to inside in March. The only change that is statistically significant is the increase in solitary ascidians.

The poor quality of the experimental design of this study is concerning as it was carried out by NIWA staff who should know more about experimental design than what has been shown in this study (one of the authors has recently co-edited a book on Marine experimental design). No misquotation of references was found.

Brown and Lamare (1994)

Brown and Lamare (1994) performed a large-scale 7 month survey of Undaria in TimaruHarbour. The following facts can be taken from Brown and Lamare’s survey.

  • Rocks in the harbour of 3-5 cm dia or smaller had no growth of Undaria, where as rocks from 5-10 cm dia did have growth of Undaria.
  • Maximum depth plants were found down too was 5m. At 5m depth the light level was 100 E with a surface PFD of 1100 E per m2. I.e. over 90% of the light was attenuated at this depth. There was suitable substrate below this depth.
  • Larger plants were at the more exposed Harbour sites. Exposure was measured with plaster balls.
  • The sporophytes disappeared by late summer.

Brown and Lamare (1994) also concluded that Undaria colonises disturbed substrata like an opportunist, but lacks other attributes associated with opportunists such as several generations per year, high fecundity and high net primary productivity. They also feel that a low competitive ability of the species is implied by its low abundance among large seaweeds, although it could possibly compete with the fucalean seaweeds, Sargassum, Cystophora, and Carpophyllum. No misquotation of references was found and statements not based on the surveys results were backed up by appropriate references.

Casas and Piriz (1996)

Casas and Piriz (1996) surveyed wharfs and ports of Puerto Madryn, Argentina, from 1992 and stated that they found that Undaria attached to substrates not covered by native seaweeds, and one of these substrata were ascidians. No misquotation of references was found and statements not based on the surveys results were backed up by appropriate references.

Castric- Fey et al. (1993)

The conclusions Castric-Fey et al. (1993) made were that Undariapinnatifida will become introduced into indigenous settlements without generating major problems to the environment. Undaria behaves relatively non aggressively against the native flora, but may compete with Sargassumpolysacharides for similar habitats. Castric-Fey et al. (1993) appears to be a large scale survey of the coast of St Malo, France. Unfortunately the methods used are not well documented so an in depth critical appraisal is hard to perform. The measurements in the survey were of numbers of algae per meter squared, which is the suggested measurement to use (see section one). No misquotation of references was found and statements not based on the surveys results were backed up by appropriate references.