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Mangrove propagule herbivory - responses and balancing interactions
Propagule herbivory may not be a threat for mangrove establishment and early growth
Thesis submitted by Van Nedervelde Fleur
in fulfilment of the requirements of the PhD Degree in Biological Sciences (ULB - “Docteur en Sciences Biologique”) and in Biologie (VUB)
Academic year 2018-2019
Supervisors: Professor Dahdouh-Guebas Farid (Université libre de
Bruxelles)
and Professor Koedam Nico (Vrij Universiteit Brussel)
Van Nedervelde Fleur
E-mail address: fleur@vannedervelde.be Phone: 0032485582963
Systems ecology and resources management Université Libre de Bruxelles
Promotors:
Prof. Dr. Farid Dahdouh-Guebas
Systems ecology and resources management Université Libre de Bruxelles
Prof. Dr. Nico Koedam
Laboratory of Plant Biology and Nature Management Vrije Universiteit Brussel
Jury members:
Prof. Dr. Olivier Hardy Prof. Dr. Ludwig Triest
Prof. Dr. Jean-Claude Grégoire Dr. Sunita Janssenswillen Prof. Dr. Sara Fratini
Prof. Dr. Satyanarayana Behara
Photographs credit: Van Nedervelde Fleur
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Chapter 1a
Summary p.5 Résumé p.7 Samenvatting p.9
Contents
References p.121 BEST OFF p.120
CHAPTER 5: GENERAL DISCUSSION AND PERSPECTIVES
Summary of findings p.107
Extrinsic and intrinsic factors p.115 Limits, future research perspectives and
applications p.117
Evidence and characteristics of tolerance p.113 Costs and benefits of herbivory on propagules
p.109
Propagule herbivory may not be a threat for mangrove establishment and early growth p.108
CHAPTER 4: CRAB HERBIVORY What regulates crab herbivory on mangrove
propagules? p.87 CHAPTER 1: INTRODUCTION
Research justifications and general objectives p.34
Once upon a time mangrove propagule p.15 Let’s disperse in the mangrove forest while
propagule predators are around p.18 Establishment and Seedling-Stalk growth p.31 Lived normally even after damage: tolerance, a
stable resistance p.33
Framework objectives p.38
CHAPTER 3: INSECT HERBIVORY AND PROPAGULE SURVIVAL
CHAPTER 2: INSECT HERBIVORY AND PROPAGULE ESTABLISHMENT
Mangrove propagules stand tolerant to insect infestation by efficiently bypassing necrosed tissues when forming adventitious roots. p.41
Boring insect herbivory, no worries, Rhizophora
mangle recovers. p.65
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Summary
One of the most critical periods in a plant’s life cycle is seedling establishment. This is even more true for mangrove seedlings that immediately after abscission have to deal with high salinity, soil hypoxia, wave action and submergence by tides. Next to abiotic constraints, mangrove propagules are commonly attacked and consumed by herbivores (propagule predators).
Part one: In Florida (USA), several insects feed on Rhizophora mangle. The most represented insect herbivore in our study region is Coccotrypes rhizophorae, a Scolytinae of about 2 millimeters long. It infests exclusively Rhizophora mangle propagules and juveniles, in our study region, by digging chambers, feeding on internal tissues and raising offspring inside. C.
rhizophorae is known to be a threat to mangrove regeneration. Nevertheless, R. mangle has a mechanism of defence, propagules may react to insect attack by producing adventitious roots just above necrosed tissues. We focused our study on this phenomenon. More specifically, we examined whether development of induced roots above an attack could offer infested propagules better chances to establish and survive (several months in light and shade in natural field conditions) (Chapter 2). In addition, we investigated how early growth (one year under controlled greenhouse conditions) could be impacted by insect damage and presence of newly induced roots (Chapter 3). Induced roots could replace normal roots and make establishment possible, even for highly damaged propagules. They increased the chances of establishment and survival of infested propagules. However, some propagules that were attacked and only slightly damaged did not form induced roots but also survived and established. Moreover, early growth is affected differentially depending on damage intensity and presence or absence of induced roots. Globally, the juvenile growth rate was inversely proportional to the amount of damage. This could be compensated by presence of induced roots, but it was not always the case. Indeed, compensation depended on which part of the propagule was attacked. Damage located on the upper part of a propagule (towards the plumule) tended to have stronger impact on early growth. Following those results, we conclude that induced adventitious roots may replace initial and / or normal roots. In certain conditions they offer to infested propagules the ability to survive, establish and grow in a same way as non-infested propagules. In that context, we can confirm that those propagules are then tolerant to insect herbivory.
Hence, depending on propagule availability, tolerance ability and degree of C. rhizophorae
infestation, the insect may be not a major threat for R. mangle regeneration.
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Part two: Crabs play a major role in mangrove ecosystems. In Gazi Bay (Kenya), some herbivorous crab families (e.g. Sesarmidae, Gecarcinidae) are known to consume propagules.
This herbivory can affect mangrove regeneration in natural and restored stands. Crab herbivory on propagules may be affected by many biotic and abiotic factors. We examined how some of the factors could determine the herbivory behavior of two cab species (Neosarmatium africanum and Neosarmatium smithi) and how those factors could stabilize herbivore- vegetation mutual interactions by answering five questions (Chapter 4). We tested whether:
(1) crab density influences propagule herbivory rate; (2) crab size influences food competition and herbivory rate; (3) crabs depredate at different rates according to propagule and canopy cover species; (4) vegetation density is correlated with crab density; and (5) food preferences of herbivorous crabs are determined by size, shape and nutritional value. We found that (1) propagule herbivory rate was positively correlated to crab density. (2) Crab competition abilities were unrelated to their size. (3) Avicennia marina propagules were removed more quickly than Ceriops tagal except under C. tagal canopies. (4) Crab density was negatively correlated with the density of A. marina trees and pneumatophores. (5) Crabs prefer small items with a lower C:N ratio.
There is a mutual relationship between stand characteristics and crab fauna, where stand composition and density influence predation and crab density, crab density impacts predation rates and crab size does not influence competition for mangrove propagules. Consequently, the mutual relationship between vegetation and crab populations seems to be important for forest restoration success and management.
We conclude that this study gives answers on how herbivore-propagule mutual relationships
are stabilized with tolerance, escape resistances and by intrinsic / extrinsic factors. However,
more research is required to investigate how these herbivore-propagule interactions may evolve
under increasing anthropic impacts, climate change and whether herbivore-propagule
interactions are altered by these impacts and changes.
Résumé
Une des périodes les plus critiques pour les plantes est l’établissement des jeunes plants. Cela est d’autant plus vrai pour les plantules de mangrove qui doivent, juste après leur abscission, gérer une haute salinité, un sol hypoxique, le courant engendré par les vagues et les marées. En plus des contraintes abiotiques, les propagules des mangroves sont souvent attaquées et mangées par des herbivores.
Partie une: En Floride (USA), plusieurs insectes se nourrissent de Rhizophora mangle.
L’insecte herbivore le plus représenté dans notre région d’étude est Coccotrypes rhizophorae, un Scolytinae d’environ 2 millimètres de long. Il infeste exclusivement les propagules et juvéniles de Rhizophora mangle, dans notre région d’étude, en creusant des galeries, en mangeant les tissues internes et en pondant ses œufs à l’intérieur. C. rhizophorae est connu pour être une menace à la régénération des mangroves. Cependant, R. mangle a un mécanisme de défense, les propagules peuvent réagir à l’attaque de ces insectes en développant des racines adventives juste au-dessus des tissues nécrosés par l’insecte. Nous avons focalisé notre étude sur ce phénomène. Plus spécifiquement, nous avons examiné si le développement de ces racines adventives au-dessus des dommages d’insectes peut offrir aux propagules infestées de meilleures chances de s’établir et de survivre (observations sur le terrain et sur plusieurs mois dans des conditions naturelles d’ombre et d’ensoleillement) (Chapitre 2).
De plus, nous avons étudié comment le début de la croissance (contrôle sur un an dans des
conditions artificielles sous serre) peut être impactée par les dommages d’insectes et par la
présence de racines adventives (Chapitre 3). Les racines adventives induites par les dommages
d’insectes peuvent remplacer les racines normales et rendre possible l’enracinement, même
pour des propagules fortement endommagées par les insectes. Ces racines augmentent les
chances d’établissement et de survie des propagules infestées. Cependant, quelques propagules
infestées ont survécu et se sont établies sans développer de racines adventives mais ces
propagules n’étaient que peu endommagées. De plus, le début de la croissance est affecté de
manière différente selon l’intensité des dommages et la présence ou absence de racines
adventives. Globalement, le taux de croissance des juvéniles était inversement proportionnel à
la quantité de dommages. Cela peut être compensé par la présence de racines adventives, mais
ce n’était pas toujours le cas. En effet, la compensation dépend de la partie attaquée. Les
dommages localisés dans la partie supérieure de la propagule (près de la plumule) tendent à
avoir un impact plus grand sur le début de la croissance. D’après nos résultats, nous pouvons
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conclure que les racines adventives induites par l’attaque peuvent remplacer les racines initiales et/ou normales. Dans certaines conditions, ces racines offrent, aux propagules infestées, la possibilité de survivre, de s’établir et de grandir de la même manière que les propagules non infestées. Dans ce contexte, nous pouvons affirmer que ces propagules sont tolérantes à l’herbivorie de cet insecte. Donc selon la disponibilité des propagules, leur habilité à être tolérante et le degré d’infestation de ces insectes, C. rhizophorae n’est peut-être pas une menace majeur pour la régénération de R. mangle.
Partie deux: À Gazi Bay (Kenya), certaines familles de crabes herbivores (e.g. Sesarmidae, Gecarcinidae) sont connues pour consommer des propagules. Cette herbivorie peut affecter la régénération des mangroves dans des forêts naturelles et restaurées. L’herbivorie des crabes sur les propagules peut être affectée par de nombreux facteurs tant biotiques qu’abiotiques.
Nous avons examiné comment certains de ces facteurs peuvent déterminer le comportement
d’herbivorie de deux espèces de crabes (Neosarmatium africanum and Neosarmatium smithi)
et comment ces facteurs peuvent stabiliser les interactions entre les herbivores et la végétation
en répondant à cinq questions (Chapitre 4). Nous avons testé si : (1) la densité des crabes
influence le taux d’herbivorie sur les propagules ; (2) la taille des crabes influence la
compétition pour la nourriture et le taux d’herbivorie ; (3) la consommation des crabes est
influencée par les espèces de propagules et de la couverture végétale ; (4) la densité de
végétation est corrélée avec la densité de crabes ; et (5) les préférences alimentaires des crabes
herbivores sont déterminées par la taille, la forme et la valeur nutritives des aliments. Nous
avons trouvé que (1) le taux d’herbivorie sur les propagules est positivement corrélé à la densité
de crabes. (2) La compétitivité des crabes n’est pas corrélée à leur taille. (3) Les propagules
d’Avicennia marina sont plus rapidement déplacées que celles de Ceriops tagal sauf sous
couvert de C. tagal. (4) La densité des crabes est négativement corrélée à la densité des arbres
d’A. marina et de ses pneumatophores. (5) Les crabes préfèrent les aliments de petites tailles
avec un ratio C:N faible. Nous avons trouvé qu’il y a une relation mutuelle entre la structure
de la végétation et les populations de crabes. La compréhension de cette relation mutuelle peut
être importante pour le succès et la gestion des forêts restaurées. Cette étude nous apprend
comment les interactions mutuelles entre herbivores et propagules se stabilisent avec des
mécanismes tels que la tolérance et la fuite ainsi que avec des facteurs intrinsèques et
extrinsèques. Cependant, des études supplémentaires sont requises pour comprendre comment
ces interactions entre herbivores et propagules peuvent évoluer avec les variations dues à la
pression anthropique et aux changements climatiques.
Samenvatting
Eén van de meest kritische periodes voor planten is de vestiging van de zaailingen. Dit is nog meer het geval voor zaailingen van mangroven, die meteen na abscissie kampen met hoge saliniteit, hypoxie in de bodem, golfenergie en getijden. Naast abiotische factoren, worden mangrovenpropagulen ook vaak aangevallen en opgegeten door herbivoren.
Deel I: In Florida (VS) voeden verscheidene insecten zich met Rhizophora mangle. De meest
voorkomende van de herbivore insecten in de bestudeerde regio is Coccotrypes rhizophorae,
een ongeveer 2 millimeter lange Scolytinae. Deze tast bijna uitsluitend Rhizophora mangle
propagulen en jonge plantjes aan, door gangen te graven in het weefsel, intern weefsel te eten
en zich binnen de propagule voort te planten. C. rhizophorae staat bekend als een bedreiging
voor de regeneratie van mangroven. Nochtans heeft R. mangle een tolerantie en
verdedigingsmechanisme. Propagulen kunnen op de aanval van insecten reageren door net
boven genecrotiseerd weefsel adventieve wortels te produceren. Onze studie richt zich op dit
fenomeen. Meer specifiek hebben wij onderzocht of de ontwikkeling van geïnduceerde wortels
boven een plaats op de propagule van een insectenaanval meer kans geeft aan aangetaste
propagulen zich te vestigen en te overleven (waarneming gedurende meerdere maanden in licht
en schaduw, natuurlijke veldomstandigheden) (Hoofdstuk 2). Tevens hebben wij bestudeerd
hoe de vroege groei (één jaar onder gecontroleerde omstandigheden in een kas in België)
beïnvloed kan worden door insectenschade en de aanwezigheid van recent geïnduceerde
wortels (Hoofdstuk 3). Geïnduceerde wortels kunnen normale wortels vervangen en de
vestiging mogelijk maken, zelfs voor zeer beschadigde propagulen. Dit vergrootte de kans op
vestiging en overleving van de aangetaste propagulen. Sommige aangetaste propagulen die
geen geïnduceerde wortels vormden, overleefden en vestigden zich daarentegen ook maar in
dat geval waren ze slechts licht beschadigd. Bovendien wordt de vroege groei differentieel
beïnvloed, afhankelijk van de intensiteit van de schade en van de aanwezigheid of afwezigheid
van geïnduceerde wortels. Over het algemeen was de juveniele groeisnelheid omgekeerd
evenredig met de hoeveelheid schade. Dit kon gecompenseerd worden door de aanwezigheid
van geïnduceerde wortels, maar dat was niet altijd het geval. De compensatie hing af van het
deel van de propagule dat aangevallen werd. Schade aan het bovenste deel van de propagule
(bij de bladaanleg, pluimpje) heeft vaak meer impact op de vroege groei. Op basis van deze
resultaten concluderen wij dat geïnduceerde incidentele wortels oorspronkelijke en/of normale
wortels kunnen vervangen. In sommige omstandigheden geven ze aangetaste propagulen de
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mogelijkheid op dezelfde manier te overleven als niet-aangetaste propagulen, zich te vestigen en te groeien. In deze context kunnen we bevestigen dat deze propagulen tolerant zijn t.o.
herbivore insecten. Daarom vormt het insect, afhankelijk van de beschikbaarheidsgraad van propagulen, van hun tolerantievermogen en van de infestatiegraad van C. rhizophorae, geen grote bedreiging voor de regeneratie van R. mangle in de onderzoek context van dit werk.
Deel II: Krabben spelen een belangrijke rol in veel mangrove-ecosystemen. Voor het veel bestudeerde gebied in Gazi Bay (Kenia), weten we dat verscheidene families (e.g. Sesarmidae, Gecarcinidae) van herbivore of omnivore krabben zich voeden met propagulen. De herbivorie kan de mangroveregeneratie van natuurlijke en herstelde mangrovebestanden beïnvloeden.
Deze krabbensoorten (die ook op propagulen foerageren) ondergaan zelf diverse invloeden van de in het systeem heersende biotische en abiotische factoren. Door vijf vragen te beantwoorden, bestudeerden wij hoe sommige van de factoren het herbivorie gedrag van twee krabbensoorten (Neosarmatium africanum en Neosarmatium smithi) kunnen bepalen en hoe die factoren de wederzijdse interactie tussen herbivoor en vegetatie kunnen stabiliseren (Hoofdstuk 4). Wij hebben getest of: (1) krabdensiteit de propagule herbivoorproportie beïnvloedt; (2) krabgrootte concurrentie en herbivoorproportie beïnvloedt; (3) schade door krabben op verschillende manieren gebeurt naargelang de verschillende propagulensoorten die gegeten worden en soorten die de boomlaag vormen; (4) vegetatiedensiteit gecorreleerd is met krabdensiteit; (5) voedingsvoorkeur van herbivore krabben bepaald wordt door grootte, vorm en nutritionele waarde (C:N ratio). We hebben geconstateerd dat (1) de proportie van herbivorie op propagulen positief gecorreleerd is met krabbendensiteit; (2) het competitief vermogen van krabben (voor herbivorie) geen verband heeft met hun grootte; (3) Avicennia marina propagulen sneller geconsumeerd worden dan die van Ceriops tagal, behalve onder bedekking van C. tagal zelf (boomlaag); (4) krabbendensiteit negatief gecorreleerd is met de densiteit van A. marina bomen en pneumatoforen (ademwortels); (5) krabben een voorkeur hebben voor kleine items met een lagere C:N ratio.
Er bestaat een wederzijdse verhouding tussen groepskenmerken en de krabbenfauna. Waar de
groepssamenstelling- en densiteit de predatie en krabbendensiteit beïnvloeden, heeft
krabbendensiteit invloed op de intensiteit van predatie. Krabgrootte heeft geen impact op
competitie voor mangrove propagulen. Bijgevolg zou de wederzijdse verhouding tussen
vegetatie en krabbenpopulatie belangrijk kunnen zijn voor het succes en het beheer van
bosrestauratie.
Deze studie geeft inzicht in de wederzijdse verhouding tussen herbivoren en propagulen en hoe deze gestabiliseerd kan worden door tolerantie, ontsnappingsmechanismen, intrinsieke en extrinsieke factoren. Meer onderzoek is echter vereist om te bepalen hoe de interactie tussen herbivoren en propagulen zou kunnen evolueren met verandering als gevolg van menselijke druk en klimaatverandering, en of de aard en de uitkomst van de interacties zelf wijzigen t.g.v.
de milieuverandering.
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Pour maman
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Introduction
Partially adapted from publication and manuscripts of chapters 2, 3 and 4.
Rhizophora mangle, Indian River, Florida
Chapter 1
Once upon a time there was a mangrove propagule
Sexual reproduction is one of the principal mechanisms that determines most living beings. It is one of the major trigger of evolution. Every living organism descends from parent or parents through vegetative or sexual reproduction. Plants are not an exception; certain species may use up to much of their storage products to increase fitness and some may die thereafter. Fitness development needs energy allocation from adult plants and progeny has not always the possibility to develop into adults. Indeed, one of the most critical phases for plants is seed dispersal and seedling establishment. Seeds need specific conditions to disperse, germinate, establish and grow. This period is crucial especially as it structures future vegetation. This statement is even more true in extreme environments limited in seed requirements such as humidity, temperature, light, space and / or nutrient availability.
Mangrove ecosystems are associated with extreme conditions since they grow along the land- sea interface in bays, estuaries, lagoons, and backwaters in tropical and subtropical regions (Mukherjee et al., 2014). This habitat between land and sea is unbalanced: salinity, soil conditions, light intensity and competition vary according to season, nyctemeral period, topography, tidal regime and phase, structure of the existing vegetation (Krauss et al., 2008) and water currents (Van der Stocken et al., 2013; 2015). Because of these conditions, many mangrove tree species have developed vivipary or cryptovivipary (Ball, 1988; Lugo and Snedaker, 1974; Macnae, 1969; Tomlinson and Cox, 2000, Tomlinson, 2016) and hence seed germination in saline environments is avoided (Joshi et al., 1972). Viviparous mangrove species have embryos that germinate and accumulate reserves, without a period of dormancy, while hanging on the parent tree before abscission and dispersal as hydrochorous propagules - the dispersal unit. In plant science, the term “propagule” is defined as: any structure that functions in propagation and dispersal as spore or seed (Allaby, 2010).
In mangrove ecosystems it is similar except that the dispersal unit of viviparous trees are
actually seedlings (Fig. 1.1). Since we did not study the fate of propagule while it is still
attached to the tree, in the rest of this dissertation, the term propagule refers to the dispersal
unit between abscission and establishment, the latter of which occurs when the plant anchors
into soil and does not disperse anymore. We assumed that propagules were established and
become seedlings when they were anchored and had at least two unfurled leaves. The
Rhizophoraceae family has the most pronounced vivipary amongst mangroves (Cheeseman,
2012), their propagules are mostly structured by a large elongated cylindrical hypocotyl topped
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by a short plumule (embryonic stem, cotyledons that remain tied to fruit during abscission) and ended by a radicle (embryonic root) (Tomlinson and Cox, 2000; Tomlinson, 2016) (Fig. 1.1;
Table 1.1). The Avicennia genus (Acanthaceae family) is cryptoviviparous, develops smaller propagules mostly structured by two large circular interlocked cotyledons surrounding the first tiny leaves, extended by a small hypocotyl ended by a radicle (embryonic root) and entirely enclosed by a fleeting periderm (Fig. 1.1, Table 1.1). Those morphologies are similar to juvenile plants developed from a seed after abscission, called seedling in plant science terms (Allaby, 2010) and that usually are, by this time, established.
The Rhizophoraceae family has some of the largest sized propagules (Fig. 1.1, Table 1.1) and are basically composed by four types of tissue from interior to exterior: the pith, the vascular tissue, the cortex and the epidermis. Pith as well as cortex cells store abundant starch grains (Tomlinson and Cox, 2000; Tonné et al., 2016), the common energy reserve of green plants.
Similarly, cotyledons of Avicennia genus, store a large quantity of reserve. This reserve and
stored water are used for propagule survival during dispersal (Robert et al., 2015) and early
growth of established seedlings (Smith and Snedaker, 2000). Quantity of reserve, size (Robert
et al., 2015), morphology characteristics and density (Van der Stocken et al., 2019) provide to
propagules a relatively large dispersal distance, abilities to survive and establish in unbalanced
habitat. Nonetheless, for a small propagule as the ones of A. germinans (L.) L., establishment
and seedling productivity are better if the period of flotation is short (Simpson et al., 2017).
Figure 1.1: Proportional pictures of propagules; a. Acanthaceae family (Avicennia marina); b.
Rhizophoraceae family (Ceriops tagal) in Gazi Bay, Kenya and c. Rhizophoraceae family (Rhizophora mangle) from Fort Pierce, Florida. #139: individual identification number.
c a
b
4 cm
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Let’s disperse in the mangrove forest while propagule predators are around.
Just after abscission, propagules may either self-plant in the soil depending on soil texture (soft, hard) and obstacles as tree branches and areal root network (Fig. 1.2) that can change velocity and orientation of fusiform propagules from the Rhizophoraceae family. Or they can fall directly in water depending on intertidal position of parent tree and tidal period when they abscise.
Figure 1.2: High dense network of pneumatophores (aerial roots); a. pencil roots of A. marina and b.
prop roots of R. mucronata in Gazi Bay, Kenya
Propagules which have not self-planted can lay on the forest floor and be transported by tidal currents if nothing withholds them. Hydrochorous propagules comprise a relatively high proportions of intercellular air spaces (Tonné et al., 2016) that provide them with floating abilities that drives dispersal.
Dispersal orientation and distance may depend on currents, winds, plant obstacles, propagule morphology and density (Van der Stocken et al., 2013; 2015) (Fig. 1.1, Table 1.1). This period is critical; propagules may never encounter a suitable habitat and the outcome of dispersal may be affected by abiotic factors, e.g. aridity / drought, salinity (Krauss et al., 2008), sediment biogeochemistry (Kristensen et al., 2008), tidal inundation (Gilman et al., 2008), topography (Di Nitto et al., 2008) and biotic factors (Lee, 1999), e.g. the vegetation assemblage (Berger et al., 2008), anthropogenic pressure (Walters et al., 2008) and interactions with fauna (Cannicci et al., 2008) (Fig. 1.3).
Herbivores have a greater impact on seeds and seedlings than they have on adult plants.
Seedlings are more vulnerable since they allocate more resources to rapid establishment and early growth than they do to defence (Duthoit, 1964; Dirzo and Harper, 1980; Fenner et al.,
a b
1999). Additionally, the same amount of damage has a greater influence on small entities, as the biomass removed is disproportional (loc. cit.) and has more risk to affect vital tissues or organs such as unique apical meristem or root-shoot connections.
Despite a large reserve storage, mangrove propagules have a low nutritive value, above the
critical value of C: N ratio (17: 1) considered to be under the nutritional requirement (Russel-
Hunter, 1970) and contain antinutritive tannins (Table 1.1). However, mangrove propagules
are commonly depredated by molluscs and arthropods (crabs, insects) (Table 1.1) (Cannicci et
al., 2008; Dahdouh-Guebas et al., 2011).
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Figure 1.3: Abiotic and biotic factors affect adult tree productivity, propagule dispersal, establishment and early growth of seedlings in a mangrove forest with an emphasis on beneficial and damaging interactions with fauna; bolded boxes are factors affecting mangrove ecosystems; factors in bolded orange are faunal impacts; non-bolded boxes are stages of mangrove life cycle; grey arrows show the life cycle path and black arrows indicate the direction of influences. We took the example of a Rhizophora sp. but it is applicable to all viviparous mangrove species. Sources: [1] Kristensen and Alongi, 2006, [2] Kristensen, 2008, [3] McNae, 1968, [4] Cannicci et al., 2009, [5,6] Lee, 1998, 2008, [7] Cannicci et al., 2008, [8] Bosire et al., 2005, [9] Cannicci et al., 2008, [10] Sousa et al., 2003a, [11]
Krauss et al., 2008, [12] Anderson and Lee, 1995, [13] Tong et al., 2003, [14] Smith and Snedaker, 2000, [14a,b] Sousa et al., 2003a,b, [15] Robertson et al., 1990, [16] Minchinton and Dalby-Ball, 2001, [17] Krauss and Allen, 2003a, [18] Van der Stocken et al., 2015, [19] Di Nitto et al., 2008, [20]
Rabinowitz, 1978a, [21] Cheeseman, 2012, [22] Van der Stocken et al., 2015, [23] Onuf et al., 1977,
[24] Elster et al., 1999, [25] Brook, 2001, [26] Van der Stocken et al., 2013, [27] Robert et al., 2015,
[28] Nagelkerken et al., 2008, [29] Robert, 2012, [30] Ellison and Farnworth, 1997, [31] Hoppe-Speer
et al., 2011, [32] Sivasothi, 2000, [33] Beever et al., 1979, [34] Berger et al., 2008
22
Herbivory on mangrove propagules may affect their survival if more than 50% of the hypocotyl are damaged, if one of the apical meristems (plumule or radicule) is lost or if propagule is buried in a crab burrow (in case of crab herbivory) (Smith, 1987a). In case of a smaller proportion of damage, initial growth of mangrove seedlings may be negatively affected by the reduction of biomass and energy reserves of hypocotyl or cotyledons (Robertson et al., 1990;
Minchinson and Dalby-Ball, 2001; Krauss and Allen, 2003a; Sousa et al., 2003a). Since establishment is a crucial point in a species’ life cycle (Hulme, 1994; Scheidel and Bruelheide, 2005), seedling eaters have a pronounced impact on the composition of plant communities (Crawley, 1989; Hulme, 1994). It was proved that herbivory on mangrove propagules can affect mangrove fitness (Onuf et al., 1977; Rabinowitz, 1977; Robertson et al., 1990; Clarcke, 1992; Farnsworth and Ellison, 1997; Elster et al., 1999; Brook 2001; Minchinton and Dalby- Ball 2001; Sousa et al., 2003 a, b) and can, under certain conditions, affect considerably mangrove regeneration (Farnworth and Ellison, 1997; Dahdouh-Guebas et al., 1998; Sousa et al., 2003a,b).
Table 1.1 Characteristics of the three mangrove propagule genera studied and related herbivory pressure. We have specific data for R. mangle, R. mucronata, C. tagal and A. marina (our research species) and if there are no data on specific species, we extend research to R. stylosa and A. germinans for Rhizophora spp. and Avicennia spp. respectively. If there are no data on propagules, we extend research on leaves, pointed out with brackets.
Sources: [1] Kathiresan and Bingham, 2001, [*] personal observations or data see chapters 3 and 4, [2]
De Ryck et al., 2012, [3] McKee, 1995c, [4] Erickson et al., 2004, [5] Micheli, 1993a, [6] Skov and
Hartnoll, 2002, [7] Smith, 1987a, [8] Basak et al., 1998, [9] Giddins et al., 1986, [10] Camilleri, 1989,
[11a,b] Sousa et al., 2003a,b, [12] Farnsworth and Ellison, 1997, [13] Dahdouh-Guebas et al., 1998,
[14] Dahdouh-Guebas et al., 1997, [15] Robertson et al., 1990, [16] refer to Chapter 4, [17] Minchinton
and Dalby-Ball, 2001, [18] Clarke, 1992, [19] Elster et al., 1999.
Characteristics Propagule species
Rhizophora spp. Ceriops spp. Avicennia spp.
Family Rhizophoraceae Rhizophoraceae Acanthaceae
Vivipary True vivipary [1] True vivipary [1] Cryptovivipary (the embryo displays no dormancy period) [1]
Shape Elongated cylinder-shaped [*] Elongated cylinder-shaped [*] Roughly spherical to ovoid, flattened with one rounded side and one flatter side [*]
Fresh weight (g) Rhizophara mangle 20,7 (SD: 6.5) [*];
Rhizophara mucronata 68.5 (SD: 10.6) [2] Ceriops tagal 7.6 (SD: 1.5) [*] Avicennia marina 3.5 (SD: 0.6) [*]
Nutritional value (C : N) R. mangle 72.6 (SE : 3.0) [3] ;
R.mangle (leaves) 36.4 [4] C. tagal (Leaves) 214 [4] – 87.89 (SE : 6.4) [5]
Avicennia germinans 36.6 (SE : 1.1) [3] ; A. germinans (leaves) 24.3 [4] ;
A.. marina (Leaves) 31.7 [5] - 46.22 (SE : 3.39) [5] -78.9 [6]
Nutritional value
(Carbohydrates) (%) Rhizophara stylosa 14.7 (SD: 4.0) [7] C. tagal 10.8 (SD: 2.6) [7] A. marina 55.6 (SD: 3.8) [7]
Nutritional value (Starch) (%) R. stylosa 23.5 (SD: 3.6) [7] C. tagal 12.0 (D: 5.9) [7] A. marina 5.9 (SD: 4.6) [7]
Gallotannins (mg) R. mangle 27 (SE: 1) [3] - A. germinans 7 (SE: 1) [3]
Condensed tannins (mg) R. mangle 646 (SE: 22) [3] - A. germinans 0 (SE: 0) [3]
Tannins (%) R. stylosa (leaves) 17.43 (SE : 2.33) [5] ; R. stylosa 14.7 (SD : 5.3) [7]
C. tagal (leaves) 11.4 (SE : 0.48) [5] ; C.tagal 24.9 (SD : 8.1) [7]
A. marina (leaves) 6.76 (SE: 0.42) [5];
A. marina 1.5 (SD: 1.0) [7]
Polyphenolics (lignin or
tannins (%, mg) R. mangle (Leaves) 23% [4];
R. mucronata (leaves) 20-23% [8] C. tagal (Leaves) 150 mg [9] A. marina (Leaves) 35 mg [10]
Herbivory pressure (%)
R. mangle 71 [*];
R.stylosa 50.4 (SD: 42.1) [7];
R. mangle 90 [11b];
R. mangle 2.1-92.9 [12];
R. mucronata 10.6 (SD: 0.8)- 20 (SD: 0.9) [13];
R. mucronata 8-86 [14]
C. tagal 0-100 [2];
C. tagal 71.7 (SD: 16.5) [7];
C. tagal 0.3-1.6 [9];
C. tagal 0.0-71.1 [12];
C. tagal 20 (SD: 1.5)- 42 (SD: 2.2) [13];
C. tagal 40-66 [14];
C. tagal 7.2-8.2 [15];
C.tagal up to 100 [16]
A. marina 96 (SD: 6.9) [7];
A. marina + / -60 [11a];
A.marina 14.6 (SD: 1.7)- 32 (SD: 2.1) [13];
A. marina 59.1-64.8 [15];
A. marina 69 [16];
A.marina up to 100 [17];
A. marina 42.1-43 [18];
A. germinans [19]
Related herbivores Crab [7],
Coccotrypes rhizophorae [11a, *];
beetles and crabs [12]
Crabs [2];
Crabs [7];
beetles and crabs [12];
insects and crabs [15];
Neosarmatium smithi [9, 16];
Crab [7];
Stenobaris sp. and Phytoliriomyza sp. [11a];
Insects and crabs [15];
Neosarmatium smithi and N. africanum [17];
Subtribe Phycitina [18];
24 Herbivorous insects
In mangrove ecosystems, herbivore insects commonly feed on leaves, on flowers / fruits / seeds or on wood (Cannicci et al., 2008). Leaf consumer impact plant productivity and reproductive output (Anderson and Lee, 1995; Tong et al., 2003; Burrows, 2003) as they reduce photosynthetic area (up to 13 % of R. stylosa and 36 % of A. marina leaf material loss (Burrows, 2003)), may affect key parts of a branch (e. g. apical buds) and leaves (Burrows, 2003) and induce reallocation of resources to compensate leaf area loss and cost of anti-herbivore defences (Cannicci et al., 2008). Insect borers damage plants by digging and consuming the inner tissues and cambium of bark, trunks, and branches of trees. This may induce leaf and branch fall in trees weakened structurally by material loss and decrease of sap translocation efficiency (Sauvard, 2004). This damage may make trees more vulnerable to disease and fungal infestation and may reduce tree productivity because of resource reallocation (Anderson and Lee, 1995; Tong et al., 2003). Herbivore insects may be the most damaging propagule consumers (Farnsworth and Ellison, 1997) especially boring insects that consume internal tissues (Farnsworth and Ellison, 1997, Minchinton and Dalby-Ball, 2001) (Fig. 1.4). Insect herbivory is common on mangrove propagules both before and after abscission (Robertson et al., 1990; Farnsworth and Ellison, 1997, Minchinton, 2006, Dahdouh-Guebas et al., 2011).
Depending on amount of damage, damage localisation and environmental resources availability (Robertson et al., 1990; Sousa et al., 2003a; Minchinton, 2006), herbivory may impact propagules and seedling survival, their establishment and early growth (Table 1.3).
Some studies reveal an insect herbivory pressure with up to 90% of killed propagules (Table 1.3) (Sousa et al., 2003b).
Figure 1.4: Coccotrypes rhizophorae a. female adult and two larvae; b. two larvae and c. gallery or chamber inside Rhizophora mangle propagule, a female adult and her progeny.
a b
c
0.4cm
0.2cm 0.1cm
