12 Annelida:The Metameric Body Form

The Samoan palolo worm (Eunice viridis) is one of approximately15,000 spe­ cies in the phylum Annelida. The palolo's 1·eproductive habits are unusual, but effective.As you will see in this chapter, "unusual" is not the exceptionfor this Chapter Outline taxonomicallychallenging phylum. 12.1 Evolutionary Perspective Relationships to Other Animals Metamerism and Tagmatization 12.2 Annelid Structure and Function 12. 1 EVOLUTIONARY PERSPECTIVE External Structure and Locomotion Feeding and the Digestive System Gas Exchange and Circulation LEARNING OUTCOMES Nervous and SensoryFunctions Excretion 1. Describe the relationships of members of the Annelida to other animal phyla. Regeneration, Reproduction, 2. Explain the benefits of metamerism for an annelid and Development 12.3 Clade (Class) Errantia Nereis (Neanthes, Alitta) At the time of the November full moon on islands near Samoa in the South Glycera Pacific, people rush about preparing for one of their biggest yearly feasts. In Fireworms just one week, the sea will yield a harvest that can be scooped up in nets and 12.4 Clade (Class) Sedentaria Tubeworms buckets (figure 12.1). Worms by the millions transform the ocean into what one Siboglinidae writer called "vermicelli soup!" Celebrants gorge themselves on worms that have Echiura been cooked or wrapped in breadfruit leaves.The Samoan palolo worm (Eunice Clade Clitel/ata 12.5 Basal Annelid Groups viridis, alternatively Palo/a viridis) spends its entire adult life in coral burrows Chaetopteridae at the sea bottom. Each November, one week after the full moon, this worm Sipuncula emerges from its burrow, and specialized body segments devoted to sexual 12.6 Further Phylogenetic Considerations reproduction break free and float to the surface, while the rest of the worm is safe on the ocean floor. The surface water is discolored as gonads release their countless eggs and sperm. The natives' feast is short lived, however; these reproductive swarms last only two days and do not recur for another year. The Samoan palolo worm is a member of the phylum Annelida (ah-nel' i-dah) (L. annellus, ring). Other members of this phylum include countless marine worms, the soil-building earthworms, and predatory leeches (table 12.1). Characteristics of the phylum Annelida include: 1. Body metameric, bilaterally symmetrical, and worm-like 2. Spiral cleavage, trochophore larvae (when larvae are present), and schizocoelous coelom formation 3. Paired, epidermal setae (chaetae) 4. Closed circulatory system 5. Dorsal suprapharyngeal ganglia and ventral nerve cord(s) with ganglia 6. Metanephridia (usually) or protonephridia

Relationships to Other Animals It has been clear for many years that Annelida is a monophyletic assemblage of marine, freshwater, and terrestrial worms. They are lophotrochozoans and, thus, share common ancestry with Mollusca, Brachiopoda, Bryozoa, Nemertea, and others Annelida: The Metameric Body Form 221

(a) (b) FIGURE 12.1 Palolo Feasts. (a) Women from the Nggela Group (Florida Islands) of the Solomon Islands use light from a torch to attract reproductive segments of Eunice viridis (family Eunicidae) during collecting. Photoreceptors on the reproductive segments elicit the response of the worms to light. (b) A swarm of worms as viewed through the lens of a diver's camera. The photograph on page 220 shows palolo worms (referred to by islanders as "odu") ready for feasting. (Pbotograpbs courte.,y of Dr. Si111011 Foale, Principle Resectrcb Fe/10111, ARC Ce11tre of Exce/le11cefor Coral Req( Studies.James Cook University, Quee11sla11d, Austmlio.)

Basal Protists Phyla

FIGURE 12.2 Evolutionary Relationships of Annelids to Other Animals. This figure shows an interpretation of the relationship of the Annelida to other members of the animal kingdom. The relationships depicted here are based on evidence from developmental and molecular biology. Annelids are placed within the Lophotrochozoa along with the Mollusca, Plathyhelminthes, Rotifera, and others (see pages xvi-xvii). The phylum includes approximately 15,000 species of segmented worms. Most of these are marine and traditionally classified into the class Polychaeta. As discussed in the text, this placement is being reevaluated based on evidence from molecular biology. The Christmas-tree worm (Spirohrcmcbus gigan/e11s) (family Serpulidae) shown here is a memher of the clade Senclentaria The spiral fans of this tube-dwelling annelid are derived from prostomial palps that surround the mouth and are specialized for feeding and gas exchange. 222 CHAPTER TWELVE

to differentiate groups within the polychaetes have been res­ TABLE 12.1 urrected to represent two major annelid clades: Errantia and CLASSIFICATION OF THE PHYLUM ANNELIDA Sedentaria. Sedentaria now includes some "polychaetes," leeches, earthworms, and even worms that were formerly Phylum Annelida (ah-nel'i-dah) considered separate phyla (Echiura and Pogonophora). Cli­ The phylum of triploblastic, coelomate animals whose members tellata is still a valid clade within the Sendentaria composed are metameric (segmented), elongate, and cylindrical or of earthworms, leeches, and a few smaller taxa. The leeches oval in cross section. Annelids have a complete digestive form a monophyletic clade (Hirudinea) within the Clitellata. tract; paired, epidermal setae; and a ventral nerve cord. The earthworms and their relatives, however, are not mono­ Approximately 15,000 species of annelids have been phyletic. Thus the name "Oligochaeta," which was formerly described. considered a subclass name within the Clitellata, should Clade (Class) Errantia (er-ran'tiah) be abandoned as a taxonomic designation. Two other Marine annelids; parapodia with prominent lobes supported groups lie outside of Sedentaria and Errantia. One of these, by internalized chaetae and ventral cirri; palps well Chaetopteridae, was formerly considered to be a family developed. Nereis, Eunice, Glycera. within the "Polychaeta." The other, Sipuncula, was another Clade (Class) Sedentaria (sed-en-ter'iah) phylum outside of Annelida. The hierarchical taxonomic­ Marine, freshwater, and terrestrial annelids; parapodia with categories associated with these clades have not been estab­ reduced lobes or parapodia lacking; setae associated lished. We treat Errantia and Sedentaria as clades with a with the stiff body wall to facilitate anchoring in tubes and burrows; palps reduced. Includes the clade Clitellata, parenthetical "class" designation, which seems a logical out­ echiruans, and siboglinids. Arenicola, Riftia, Lumbricus, come of ongoing and future research. Hirudo Chapter 12 is now organized to reflect this new phylo­ Other Annelid Taxa genetic work. In the next section, we describe metamerism Sipuncula (si-pun'ku-lah) and tagmatization. This discussion is followed by coverage Marine; unsegmented body; retractable anterior trunk of annelid structure and function. The term "polychaete" is called an introvelt. Formerly phylum Sipuncula. Inclusion used in a nontaxonomic sense to refer to a host of marine of this group within the Annelida remains somewhat annelids (both errantians and sedentarians) when adap­ controversial. Themiste. tations related to their common marine habitat result in Chaetopteridae (ke-top-ter' ida) similar structures and functions. After the basics of anne­ Marine; three-palt body; lives in a U-shaped tube, lid structure and function are discussed, the two major appendages for feeding and creating water currents. annelid clades and the two outlying groups are described. Chaetoptei·us. Since members of the clade Clitellata are different in many respects from other sedentarians, unique aspects of their structure and function are described in the section on Sed­ entaria. As always, this chapter ends with "Further Phyloge­ netic Considerations." (figure 12. 2 and see chapters 10 and 11). Our understanding of phylogeny within the phylum, however, has a history of contentious debate. The application of modern phylogenetic analysis is helping unravel the annelid taxonomic-tangle. Metamerism and Tagmatization Anyone who has followed the debates involved with elu­ Earthworm bodies are organized into a series of ringlike seg­ cidating annelid phylogeny will have a better appreciation ments. What is not externally obvious, however, is that the of the dynamics within the field of animal taxonomy. These body is divided internally as well. Segmental arrangement of debates underscore the importance of taxonomy in helping body parts in an animal is called metamerism (Gr. meta, zoologists understand the evolution of bilateral morphology after + mere, part). (see the discussion of metamerism and tagmatization in the Metamerism profoundly influences virtually eve1y next section). aspect of annelid structure and function, such as the anatomi­ Previous editions of this book described the Annelida cal arrangement of organs that are coincidentally associated as being composed of two classes: Polychaeta (marine with metamerism. For example, the compartmentalization worms) and Clitellata (leeches, earthworms, and others). of the body has resulted in each segment having its own While "Polychaeta" was rightly described as being paraphy­ excreto1y, nervous, and circulato1y structures. In most mod­ letic, recent molecular phylogenetic work has shown that ern annelids two related functions are probably the primary the entire annelid assemblage is encompassed by what was adaptive features of metamerism: flexible support and effi­ being called "Polychaeta." As will be discussed in more cient locomotion. These functions depend on the metameric detail at the end of this chapter, "Polychaeta" has been arrangement of the coelom and can be understood by exam­ revealed to be synonymous with Annelida, and the former ining the development of the coelom and the arrangement of should be discarded as a class name. Two older terms used body-wall muscles. Annelida: The Metameric Body Form 223

During embryonic development, the body cavity of each segment. In addition, some marine annelids have oblique annelids arises by a segmental splitting of a solid mass of muscles, and the leeches have dorsoventral muscles. mesoderm that occupies the region between ectoderm and One advantage of the segmental arrangement of coe­ endoderm on either side of the embryonic gut tract. Enlarge­ lomic spaces and muscles is the creation of hydrostatic com­ ment of each cavity forms a double-membraned septum on partments, which allow a variety of advantageous locomotor the anterior and posterior margins of each coelomic space and supportive functions not possible in nonmetameric ani­ and dorsal and ventral mesenteries associated with the diges­ mals that use a hydrostatic skeleton. Each segment can be tive tract (figure 12.3). controlled independently of distant segments, and muscles Muscles also develop from the mesodermal layers associ­ can act as antagonistic pairs within a segment. The constant ated with each segment. A layer of circular muscles lies below volume of coelomic fluid provides a hydrostatic skeleton the epidermis, and a layer of longitudinal muscles, just below against which muscles operate. Resultant localized changes the circular muscles, runs between the septa that separate in the shape of groups of segments provide the basis for swimming, crawling, and burrowing. A second advantage of metamerism is that it lessens the Endoderm Mesoderm impact of injury. If one or a few segments are injured, adjacent segments, set offfrom injured segments by septa, may be able to maintain nearly normal functions, which increases the likelihood that the worm, or at least a part of it, will survive the trauma. A third advantage of metamerism is that it permits the modification of certain regions of the body for specialized functions, such as feeding, locomotion, and reproduction. The specialization of body regions in a metameric animal is called tagmatization (Gr. tagma, arrangement). The special­ ization of posterior segments of the palolo worm for repro­ Ectoderm ductive functions (see figure 12.1) is an example of annelid tagmatization. Metamerism is not unique to the Annelida. It is also present in the Arthropoda (insects, arachnids, and their relatives) and Chordata (vertebrates, including humans). Interestingly metamerism is absent in the annelid taxa Echi­ ura and Sipuncula. It was probably lost in these lineages. This evolutionary convergence of the metameric body form in these three very successful phyla means that one or more of the previously described advantages have been a major influence in the evolution of animal body forms. Coalom

SECTION REVIEW 12.1 Members of the phylum Annelida are the segmented worms. They are lophotrocozoans and thus share ancestry with the molluscs, nemerteans, rotifers, and others. Annelid bodies are metameric. Metamerism results in separate hydrostatic compart­ ments, reduces the impact of injury, and permits tagmatization.

How bas evidence from molecular biology forced the Ventral mesentery Septum reevaluation of classification of the Annelida? FIGURE 12.3 Development of Metameric, Coelomic Spaces in Annelids. ANNELID STRCCTURE (a) A solid mesodermal mass separates ectoderm and endoderm 12.2 in early embryological stages. (b) Two cavities in each segment AND FUNCTIO� form from the mesoderm splitting on each side of the endoderm (schizocoelous coelom formation). (c) These cavities spread in all directions. Enlargement of the coelomic sacs leaves a thin layer LEARNING OUTCOMES of mesoderm applied against the outer body wall (the parietal 1. Explain how metamerism influences the biology of peritoneum) and the gut tract (the visceral peritoneum), and dorsal and ventral mesenteries form. Anterior and posterior expansion annelid worms. of the coelom in adjacent segments forms the double-membraned 2. Compare the closed circulatory system of an annelid septum that separates annelid metameres. worm to the open circulatory system of a bivalve mollusc. 224 CHAPTER TWELVE

Polychaetes are mostly marine, and are usually between 5 and The prostomium (Gr. pro, before + stoma, mouth) of 10 cm long. Polychaetes have adapted to a variety of habitats. a polychaete is a lobe that projects dorsally and anteriorly to Errantian polychaetes live on the ocean floor, under rocks the mouth and contains numerous sensory structures, including and shells, and within the crevices of coral reefs. Many mem­ eyes, antennae, palps, and ciliated pits or grooves, called nuchal bers of both major annelid clades are burrowers and move organs. The palps of some sedentarians are highly modified through their substrate by peristaltic contractions of the body into filtering fan-like structures (see figures 12.2 and 12.12). waIT:- A bucket of imertidal :;;an I normallyyielcfs vast numoers The fiisCfoaysegment,- theperistomium (Gr. peii:arounci)-, - and an amazing variety of these burrowing annelids. Many surrounds the mouth and bears sensory tentacles or cirri. sedentarians construct tubes of cemented sand grains or The epidermis of annelids consists of a single layer of secreted organic materials. Mucus-lined tubes serve as pro­ columnar cells that secrete a protective, nonliving cuticle. tective retreats and feeding stations. Other annelids, like Some annelids have epidermal glands that secrete lumines­ oligochaetes and leeches, have adapted to freshwater and ter­ cent compounds. restrial environments. Various species of errantian annelids are capable of Sedentarians and errantians share many features of walking, fast crawling, or swimming. To enable them to do structure and function because they share a common ances­ so, the longitudinal muscles on one side of the body act try. On the other hand, adaptations to diverse environments antagonistically to the longitudinal muscles on the other within these groups mean that there are many variations on side of the body so that undulatory waves move along the the annelid theme. These common features, and many varia­ length of the body from the posterior end toward the head. tions, will be described as we progress through this section. The propulsive force is the result of parapodia and setae acting against the substrate or water. Parapodia on opposite sides of the body are out of phase with one another. When External Structure and Locomotion longitudinal muscles on one side of a segment contract, the parapodial muscles on that side also contract, stiffening the In addition to metamerism, the most distinctive feature of parapodium and protruding the setae for the power stroke many annelids is the presence of lateral extensions called (figure 12.5a). As a polychaete changes from a slow crawl to parapodfa (Gr. para, oeside podion, little foot) (figure 12.4). + swimming, the period and amplitude of undulatory waves In the Errantia, chitinous rods support the parapodia, and increase (figure 12.5b). numerous setae project from the parapodia. Parapodia are Burrowing sedentarians push their way through sand reduced or absent (clade Clitellata) in the Sedentaria. Setae and mud by contractions of the body wall or by eating their are present in most sedentarians but they are in closer prox­ way through the substrate. In the latter, the annelids digest imity to the body wall. (Setae are absent in most leeches.) organic matter in the substrate and eliminate absorbed and Setae (L. saeta, bristle) (also called chaetae) are bristles undigestible materials via the anus. secreted from invaginations of the distal ends of parapodia. They aid locomotion by digging into the substrate (Errantia) and also hold a worm in its burrow or tube (Sedentaria). Feeding and the Digestive System The digestive tract of most annelids is a straight tube that mesenteries and septa suspend in the body cavity. The ante­ rior region of the digestive tract is modified into a proboscis that special protractor muscles and coelomic pressure can eve1t through the mouth. Retractor muscles bring the probos­ cis back into the peristomium. In some, when the proboscis is everted, paired jaws are opened and may be used for seiz­ ing prey. Predatory species may not leave their burrow or coral crevice. When prey approaches a burrow entrance, the worm quickly extends its anterior portion, everts the probos­ cis, captures prey with its jaws, and pulls the prey back into the burrow. Some annelids have poison glands at the base of the jaw. Other annelids are herbivores and scavengers and use jaws for tearing food. Deposit-feeding polychaetes (e.g., Arenicola, the sedentarian lugworm) extract organic matter from the marine sediments they ingest. The digestive tract consists of a pharynx that, when everted, formsthe proboscis; a storage sac, called a crop; a grinding gizzard; and a long, FIGURE 12.4 straight intestine (see figure 12.12). Organic matter is digested Clade Errantia. External structure of Nereis virens. Note the extracellularly, and the inorganic particles are passed through numerous parapodia. the intestine and released as "castings." Annelida: The Metameric Body Form 225

Longitudinal muscles relaxed Longitudinal muscles and incompletely stretched fully stretched

Parapodial muscles relax, resulting in withdrawal of --.ar Longitudinal muscles parapodia and setae fully contracted

Longitudinal muscles fully contracted --+- Points of contact with substrate or medium

Parapodial muscles contract, protruding Longitudinal muscles parapodia and setae fully stretched (a)

6-8 segrnents average 14 segmen1s "wavelength" "wavelength" 1 40 segmerils "wavelength"

(b) Slow walking Rapid crawling Swimming FIGURE 12.5 Annelid Locomotion. (a) Dorsal view of a primitive errantian annelid, showing the antagonism of longitudinal muscles on opposite sides of the body and the resultant protrusion and movement of parapodia. (b) Both the period and amplitude of locomotor waves increase as the annelid changes from a "slow walk" to a swimming mode. From: ''.ALIFE OF INVERTEBRATES"© 1979 w. D. Russell-Hunter.

Many sedentary and tube-dwelling polychaetes are fil­ other organic compounds. This method of feeding occurs in ter feeders. They usually lack a proboscis but possess other other animal phyla, too, but rarely accounts formore than 1 % specialized feeding structures. Some tube dwellers, called fan­ of their energy needs. worms, possess radioles that form a spiral-shaped or funnel­ shaped fan (see figures 12.2 and 12.12). Cilia on the radioles circulate water through the fan, trapping food particles. Gas Exchange and Circulation Trapped patticles are carried along a food groove at the axis of the radiole. During transpott, a so1ting mechanism rejects The respiratory gases of most annelids simply diffuse across the largest particles and transports the finest particles to the the body wall, and parapodiaincrease the surface area for these mouth. Another filter feeder, Chaetopterus, lives in a U-shaped exchanges. In many annelids, parapodial gills further increase tube and secretes a mucous bag that collects food patticles, the surface area for gas exchange. which may be as small as 1 µm. The parapodia of segments 14 Annelids have a closed circulatory system. Oxygen is through 16 are modified into fans that create filtration currents. usually carried in combination with molecules called respi­ When full, the entire mucous bag is ingested (see.figure 12.22). ratory pigments, which are usually dissolved in the plasma Elimination of digestive waste products can be a prob­ rather than contained in blood cells. Blood may be color­ lem for tube-dwelling polychaetes. Those that live in tubes less, green, or red, depending on the presence and/or type of that open at both ends simply have wastes carried away by respirat01y pigment. water circulating through the tube. Those that live in tubes Contractile elements of annelid circulatory systems con­ that open at one end must turn around in the tube to def­ sist of a dorsal aorta that lies just above the digestive tract ecate, or they may use cilia1y tracts along the body wall to and propels blood from rear to front, and a ventral aorta that carry feces to the tube opening. lies ventral to the digestive tract and propels blood from front Polychaetes that inhabit substrates rich in dissolved to rear. Running between these two vessels are two or three organic matter can absorb as much as 20 to 40% of their sets of segmental vessels that receive blood from the ventral energy requirements across their body wall as sugars and aorta and break into capillary beds in the gut and body wall. 226 CHAPTER TWELVE

Gut wall capillaries Circumpharyngeal Segmental Lateral Anterior connective ganglia nerves Dorsal blood

-Setae

Sensory -E---'11 Parapodium projections

Giant fibers FIGURE 12.6 Circulatory System of a Polychaete. Cross section through the body and a parapodium. In the closed circulatory system shown here, blood passes posterior to anterior in the dorsal vessel and anterior to posterior in the ventral vessel. The direction of blood flow is indicated by black arrows. Capillary beds interconnect Small fibers dorsal and ventral vessels. (b) ,______, FIGURE 12.7 Annelid Nervous System. (a) Connectives link suprapha1yngeal Capillaries coalesce again into segmental vessels that deliver and subpha1yngeal ganglia. Segmental ganglia and lateral nerves blood to the dorsal aorta (figure 12.6; see figures 12.17 occur along the length of the worm. (b) Cross section of the ventral and 12.18). ne1ve cord, showing giant fibers.

nerve impulses at 30 m/s (as opposed to 0.5 m/s in the Nervous and Sensory Functions smaller, 4-µm-diameter annelid fibers). Ne1vous systems are similar in virtually all annelids. The Annelids have various senso1y structures. Two to four annelid nervous system includes a pair of suprapharyngeal pairs of eyes are on the surface of the prostomium. They ganglia, which connect to a pair of subpharyngeal ganglia by va1y in complexity from dermal photoreceptor cells; to sim­ circumpha1yngeal connectives that run dorsoventrally along ple cups of receptor cells; to structures made up of a cornea, either side of the pharynx. A double ventral nerve cord runs lens, and vitreous body. Most polychaetes react negatively to the length of the worm along the ventral margin of each coe­ increased light intensities. Fanworms, however, react nega­ lomic sp,:ice, ,:ind a pairc>d segmental g:mglion i.-, in earh seg­ tively to decreasing light intensities. If shadows cross them, ment. The double ventral ne1ve cord and paired segmental fanworms retreat into their tubes. This response is believed to ganglia may fuse to va1ying extents in different taxonomic help protect fanworms from passing predators. Earthworms groups. Lateral nerves emerge from each segmental ganglion, lack well-developed eyes, which is not surprising, given their supplying the body-wall musculature and other structures of subterranean lifestyle. They do possess a dermal light sense that segment (figure 12.7a). that arises from photoreceptor cells scattered over dorsal and Segmental ganglia coordinate swimming and crawling lateral surfaces of the body. Scattered photoreceptors mediate movements in isolated segments. (Anyone who has used por­ a negative phototaxis in strong light (evidenced by move­ tions of worms as live fish bait can confirm that the head ment away from the light source) and positive phototaxis in end-with the pharyngeal ganglia-is not necessa1y for coor­ weak light (evidenced by movement toward the light source). dinated movements.) Each segment acts separately from, Other sense organs mediate responses to chemicals, grav­ but is closely coordinated with, neighboring segments. The ity, and touch. Nuchal organs are pairs of ciliated sensory pits or subphatyngeal ganglia help mediate locomotor functions slits in the head region. Neives from the suprapha1yngeal gan­ requiring coordination of distant segments. The suprapharyn­ glia inne1vate nuchal organs, which are thought to be chemo­ geal ganglia probably control motor and sensory functions receptors for food detection. Statocysts are in the head region involved with feeding, and sens01y functions associated with of polychaetes, and ciliated n1bercles, ridges, and bands, all of forward locomotion. which contain receptors fortactile senses, cover the body wall. In addition to small-diameter fibers that help coordi­ nate locomotion, the ventral nerve cord also contains giant fibers involved with escape reactions (figure 12.7b). For Excretion example, a harsh stimulus, such as a fishhook, at one end Annelids excrete ammonia, and because ammonia diffuses of a worm causes rapid withdrawal from the stimulus. Giant readily into the water, most nitrogen excretion probably fibers are approximately 50 µm in diameter and conduct occurs across the body wall. Excret01y organs of annelids are Annelida: The Metameric Body Form 227 more active in regulating water and ion balances, although these abilities are limited. Most marine annelids, if presented with extremely diluted seawater, cannot survive the osmotic influx of water and the resulting loss of ions. The evolu­ tion of efficient osmoregulato1y abilities has allowed only a few polychaetes to invade freshwater. Freshwater annelids excrete copious amounts of ve1y dilute urine, although they retain vital ions, which is important for organisms living in environments where water is plentiful but essential ions are limited. In addition to ammonia, earthworms excrete urea, a less toxic nitrogenous waste. The excretory organs of annelids, like those of many invertebrates, are called nephridia. Annelids have two types Protonephridium Metanephridium a of nephridia. A protonephridium consists of a tubule with a ( ) (b) closed bulb at one end and a connection to the outside of the body at the other end. Protonephridia have a tuft of flagella in their bulbular end that drives fluids through the tubule (figure 12.8a; see also figure 10.6). Some primitive annelids possess paired, segmentally arranged protonephridia that have their bulbular end projecting through the anterior sep­ tum into an adjacent segment and the opposite end opening through the body wall at a nephridiopore. Most annelids possess a second kind of nephridium, called a metanephridium. A metanephridium consists of (c) an open, ciliated funnel, called a nephrostome, that projects through an anterior septum into the coelom of an adjacent seg­ ment. At the opposite end, a tubule opens through the body wall at a nephridiopore or, occasionally, through the intestine Ventral (figure 12.Sb and c). There is usually one pair of metane­ blood vessel phridia per segment, and tubules may be extensively coiled, with one portion dilated into a bladder. A capillary bed is usu­ ally associated with the tubule of a metanephridium for active transp01t of ions between the blood and the nephridium (figure 12.Sd; see alsofigures 12.17 and 12.18). Nephrostome Most annelids have chloragogen tissue associated with the digestive tract. Chloragogen tissue surrounds the dorsal blood vessel and lies over the dorsal surface of the intes­ tine (see figure 12.13). Chlorogogen tissue acts similarly to the vertebrate liver in that it deaminates amino acids and, in earthworms, converts ammonia into urea. It also converts excess carbohydrates into energy-storage molecules of glyco­ I External opening gen and fat. (d) FIGURE 12.8 Annelid Nephridia. (a) Protonephridium. The bulbular ends of this nephridium contain a tuft of flagella that drives wastes Regeneration, Reproduction, to the outside of the body. In primitive annelids, a gonoduct and Development (coelomoduct) carries reproductive products to the outside of the body. (b) Metanephridium. An open ciliated funnel (the Many annelids have remarkable powers of regeneration. nephrostome) drives wastes to the outside of the body. (c) In They can replace lost parts, and some species have break modern annelids, the gonocluct and the nepbridial tubules undergo points that allow worms to sever themselves when a predator va1ying degrees of fusion. Cd) Nephriclia of modern annelids are grabs them. Lost segments are later regenerated. closely associated with capillary beds for secretion, and nephriclial tubules may have an enlarged bladder. From: "A L!Fh'OF INVERTEBRATES" Some polychaetes reproduce asexually by budding or © 1979 W. D R11ssell-H1111ter. by transverse fission; however, sexual reproduction is much more common. Most polychaetes are dioecious. Gonads segments. Gametes are shed into the coelom, where they develop as masses of gametes and project from the coelo­ mature. Mature female worms are often packed with eggs. mic peritoneum. Primitively, gonads occur in every body seg­ Gametes may exit worms by entering nephrostomes of meta­ ment, but most polychaetes have gonads limited to specific nephridia and exiting through the nephridiopore, or they may 228 CHAPTER TWELVE

be released, in some polychaetes, after the worm ruptures. In Prostomium these cases, the adult soon dies. Only a few polychaetes have with ganglion separate gonoducts, a condition believed to be primitive (see Peristomium figure 12.Ba-c). ,.,.,,:---nr Connective Mouth Fertilization is external in most polychaetes, although Two ciliated a few species copulate. A unique copulato1y habit has bands been reported in Platynereis megalops from Woods Hole, Massachusetts. Toward the end of their lives, male and (a) Ventral female worms cease feeding, and their intestinal tracts begin to degenerate. At this time, gametes have accumulated in the body cavity. During sperm transfer, male and female worms coil together, and the male inserts his anus into the mouth of the female. Because the digestive tracts of the worms have degenerated, sperm transfer directly from the male's coelom (c) to the egg-filled coelom of the female. This method ensures Budding fertilization of most eggs, after which the female sheds eggs metameric Anus from her anus. Both worms die soon after copulation. segments (b) Epitoky is the formation of a reproductive individual (an epitoke) that differs from the nonreproductive form of FIGURE 12.9 the species (an atoke). Frequently, an epitoke has a body that is modified into two body regions. Anterior segments cany Polychaete Development. (a) Trochophore. (b) A later planktonic larva, showing the development of body segments. As more on normal maintenance functions, and posterior segments segments develop, the larva settles to the substrate. (c) Juvenile are enlarged and filled with gametes. The epitoke may have worm. From: ''.ALIFE OF INVERTEBRATES"© 1979 U'I.D. Russell-Hunter. modified parapodia for more efficient swimming. This chapter begins with an account of the reproductive swanning habits of Eunice viridis (the Samoan palolo worm) SECTION REVIEW 12.2 and one culture's response to those swarms. Similar swarm­ Most annelids are marine worms. They are characterized by the ing occurs in other species, usually in response to changing presence of parapodia with numerous setae on most body seg­ light intensities and lunar periods. The Atlantic palolo worm, ments. Parapodia are used in locomotion and burrowing. Para­ for example, swarms at dawn during the first and third quar­ podia are reduced in size in some sedentarians and absent in ters of the July lunar cycle. others. Setae are similarly reduced. Annelids have diverse feed­ Zoologists believe that swarming of epitokes accom­ ing habits ranging from deposit to filter feeding. Annelids have plishes at least three things. First, because nonreproductive a closed circulatory system and a ventral nervous system includ­ individuals remain safe below the surface waters, predators ing segmental ganglia and nerves. Excretion usually occurs via r cannot devastate an entire population. Second, external fer­ segmental metanephridia, v, hich open through the body V\rall. tilization requires that individuals become reproductively Polychaetes are dioecious but may reproduce asexually. Sexual active at the same time and in close proximity to one another. reproduction usually occurs via external fertilization and the Swarming ensures that large numbers of individuals are in the development of trochophore larvae. Annelids within the clade right place at the proper time. Third, swarming of vast num­ Clitellata are monoecious and have direct development. bers of individuals for brief periods provides a banquet for predators. However, because vast numbers of prey are avail­ Why does the association of a capillary bed with a able for only short periods during the year, predator popula­ metanephridium provide more efficient waste process­ tions cannot increase beyond the limits of their normal diets. ing as compared to the function of a protonephridium? Therefore, predators can dine gluttonously and still leave epi­ tokes that will yield the next generation of animals. Spiral cleavage of fertilized eggs may result in planktonic 12. CLADE ( LAS ) trochophore larvae that bud segments anterior to the anus. Lar­ vae eventually settle to the substrate (figure 12.9). As growth Err, proceeds, newer segments continue to be added posteriorly. Thus, the anterior end of a polychaete is the oldest end. Many LEARNING OUTCOMES other polychaetes lack a trochophore and display direct devel­ 1. Describe the life histories of Nereis and Glycera. opment or metamorphosis from another larval stage. 2. Hypothesize on the importance of the timing and Sexual reproduction within the clade Clitellata is mark­ occurrence of reproductive swarming in many errantians. edly different from that described above. These worms are monoecious and have direct development (no larval stages) Members of the clade Errantia are mostly marine annelids. within a cocoon. These differences will be described later. They have parapodia with prominent lobes, relatively long Annelida: The Metameric Body Form 229 setae, and well developed palps. These features are adapta­ commercial bait suppliers based along the Atlantic coast of tions for active, mobile lives. Errantians comprise the majority Canada and Maine. Glycera is called the bloodworm because of the Annelida. The Samoan palolo worm (Eunice viridis) (see of the presence of hemoglobin-containing coelomocytes dis­ page 220 and.figure 12.1) is a member of the clade Errantia. tributing oxygen throughout the body cavity. Septa separating metameric compartments are incomplete; thus, the coelom Nereis (Neanthes, Alitta) is continuous through the length of the worm, and body­ wall movements are responsible distributing coelomocytes Sandworms, ragworms, and clam worms are all common and metabolic products through the body. Protonephridia are names for an annelid genus studied in general zoology lab­ used in excretion since there is no pumping vessel or other oratories as representative annelids (see figure 12.4). Some vasculature required for the function of metanephridia. authorities recognize the name Neanthes, and others the name Glycerids burrow in soft sediments and feed on small Alitta, as the valid senior synonym for this genus. There are marine invertebrates. They have a large eversible proboscis numerous species in this genus that are similar in appearance that is tipped with four jaws. The proboscis is used in bur­ and biology. Most species burrow in sand and mud of temper­ rowing and, in combination with the jaws, in capturing prey. ate marine habitats and have been collected from depths up to Reproduction follows a pattern similar to that described 90 m. Nereis virens (see figure 12.4) is common in mudflats for Nereis. Glycera reproduces once in its lifetime, and repro­ where it reaches lengths greater than 40 cm. Clam worms spend ductive swarms are correlated to the lunar cycle. Gametes are most of the daylight hours in mucus-lined burrows and emerge released into the body cavity. When worms are gravid the at night to feed. They use their eversible proboscis and large body walls of both sexes rupture, and gametes are released jaws to feed on marine vegetation and to capture nematodes for external fertilization and the development of trochophore and small arthropods. Clam worms, like most polychaetes, larvae. Obviously, the adults do not survive their brief repro­ reproduce only once during their life, and reproduction is cor­ ductive flurry. related with the lunar cycle. Males and females metamorphose into a reproductive (epitoke) stage. Using enlarged swimming parapodia, the worms swim to the surface in large numbers Fi rewarms and spawn gametes through breaks in their body walls. Adults Fireworms comprise a variety of genera within the Errantia die after releasing gametes. Fertilization results in the devel­ (family Amphinomidae). They feed on soft and hard coral opment of trochophore larvae and then juvenile worms (see polyps and small crustaceans. Eurythoe is a common genus figure 12.9). Although these worms are cosmopolitan, at least that occurs in the Caribbean and other oceans of the world one species (Nereis virens) is threatened from overharvesting (figure 12.11). The white setae fringing this annelid are hol­ by bait collectors. Attempts are currently underway to raise low and venom-filled. The setae easily penetrate the skin of clam worms commercially for the bait industry. a careless swimmer or predator, and a powerful neurotoxin causes pain, redness, and swelling. The bright colors of fire­ Glycera worms are an example of aposematic (warning) coloration (see chapter 6). Some species are bioluminescent and use There are a variety of species within the genus Glycera (figure 12.10). Like Nereis, Glycera is studied in general zoology laboratories because it is readily available from

FIGURE 12.11 Clade Errantia. The orange fireworm (Eurythoe complanta) is FIGURE 12.10 found in the Caribbean. It is shown here feeding on coral polyps. Clade Errantia. Bloodworms (Glycera) are common burrowing The white setae along the margins of the worm are hollow and errantians. venomous. 230 CHAPTER TWELVE

light in mating. Females secrete a bioluminescent protein that a crown of arm-like radioles from the open end of the tube creates a glowing green mucus coating over the worm. This (figure 12.12). Cilia1y currents move water upward through the secretion occurs during a precisely timed swarming that is radioles and organic particles are trapped in mucus. Cilia then triggered by the lunar cycle and apparently attracts males for move the food particles toward the base of the radioles to the spawning. Juvenile worms produce bioluminescent flashes mouth. Christmas tree worms (Serpulidae) use ciliary feeding that are thought to distract predators. in a similar fashion (see figure 12.2). Other tube worms that live in burrows extract organic matter from marine sediments by sweeping tentacles through the sediment or creating water SF.C.TTON REVIEW 12.3 currents that bring organic matter into their hurrow. Nereis and Glycera are representative errant annelids. They are marine predators that burrow in sand and mud during much of their lives. They use an eversible proboscis and Siboglinidae jaws in preying on small marine invertebrates. Both worms Siboglinids (beardworms) consist of about 120 species of undergo reproductive swarming that is correlated to the lunar tube-dwelling marine worms (figure 12.13). Formerly clas­ cycle. Fireworms feed on coral polyps and small crustaceans. sified into the phylum Pognophora, members of this group Their venomous setae can inflict painful stings. are now formally annelids within the polychaete family How is the method of gamete release during spawning of both Nereis and Glycera different from that of some other polychaete annelids?

12.4 CL (C :.DENf A

LEARNING OUTCOMES 1. Contrast the clades Errantia and Sedentaria. 2. Compare the oligochaete body form and the leech body form. 3. Compare and contrast the methods of fertilization and development of Nereis with members of the clade Clitellata.

Members of the clade Sedentaria include a variety of marine tubeworms, the siboglinids, the echiurans, and members of the clade Clitellata. The latter includes the leeches (Hirudinea), which is a monophyletic taxon. It also includes a variety of terrestrial and freshwater annelids formerly referred to as a subclass "Oligochaeta." The oligochaetes are not monophy­ letic, thus the name is used here to designate a variety of taxa within Clitellata that display some common structural and functional features. Sedentarians have parapodia with reduced lobes, or parapodia are completely lacking. Setae are closely associated with the stiff body wall to facilitate anchor­ ing in tubes and burrows, and palps are reduced.

Tube-worms The common name, tubeworm, is applied to a variety of sedentarian taxa that construct tubes, which are parchment­ FIGURE 12.12 like, calcareous, or composed of cemented sand grains. Oth­ Clade Sedentaria. The social featherduster (Bispira brunnea) is a ers construct burrows in sand or mud. Some tubeworms feed member of the family Sabellidae and is native to the Caribbean Sea. Cilia on the tentacle-like radioles protruding from the tube opening on particulate matter in sea water using cilia and mucus to produce water currents that trap suspended food particles. The cilia trap and transport suspended organic matter. Featherduster or then transport the food particles to the mouth of the worm located fanworms (Sabellidae) construct parchment tubes and protrude at the bases of the radioles. Annelida: The Metameric Body Form 231

FIGURE 12.13 Clade Sedenatria. Siboglinids were formerly considered to comprise a phylum, Pogonophora. The giant red siboglinid, Riftia, FIGURE 12.14 is shown here inside their tubes. Clade Sedentaria. Echiurans were originally classified as annelids and later reclassified within their own phylum. They are now likely Siboglinidae. Their tubes are embedded in soft marine sedi­ returning to the Annelida. This photograph shows the proboscis of ments in cold, deep (over 100 m), and nutrient-poor waters. an echiuran extending from a burrow. Siboglinids have no mouth or digestive tract. Nutrient uptake is via the outer cuticle and from endosymbiotic bacteria that leave their burrows. In hot, dry weather, they may retreat to siboglinids harbor in the posterior part (trophosome) of the depths of 3 m below the surface. The soil-conditioning habits body. These bacteria fix carbon dioxide into organic com­ of earthworms are well known. Lumbricus terrestris is com­ pounds that both the host and the symbiont can use. monly used in zoology laboratories because of its large size. It was introduced to the United States fromnorthern Europe and Echiura has flourished. Common native species like Eisenia foetida and various species of Allolobophora are smaller. Echiurans (spoon worms) consist of about 130 species of animals that burrow in the mud or sand of shallow marine External Structure and Locomotion Oligo­ waters throughout the world. Some live protected in rock chaetes (Gr. oligos, few + chaite, hair) have setae, but crevices. Their bodies are covered only by a thin cuticle. As fewer than are found in polychaetes (thus, the derivation of a result, the animals keep to the safety of their burrows or the class name). Earthworms lack parapodia because para­ crevices even when feeding (figure 12.14). An echiuran feeds podia and long setae would interfere with their burrowing by sweeping organic material into its spatula-shaped probos­ lifestyles. Lumbricus does have short setae associated with cis (thus the name "spoon worm"). Individual echiurans are its integument. The prostomium consists of a small lobe or from 15 to 50 cm in length, but the extensible proboscis may cone in front of the mouth and lacks sensory appendages. increase their length up to 2 m. Unlike most annelids, echiu­ A series of segments in the anterior half of an oligochaete rans are not segmented. is usually swollen into a girdlelike structure called the clitellum that secretes mucus during copulation and forms Clade Clitellata a cocoon (figure 12.15). Oligochaete locomotion involves the antagonism of cir­ Members of the clade Clitellata (kli-te'la-tah) (L. clitellae, sad­ cular and longitudinal muscles in groups of segments. Neurally dle) include the earthworms, other "oligochaetes," and the controlled waves of contraction move from rear to front. leeches. Cladistic studies have established that the presence Segments bulge and setae protrude when longitudinal of a clitellum used in cocoon formation, monoecious direct muscles contract, providing points of contact with the burrow development, and few or no setae are symplesiomorphic wall. In front of each region of longitudinal muscle contrac­ characters of this clade. Molecular data have provided ve1y tion, circular muscles contract, causing the setae to retract, strong support for the monophyly of the Clitellata. and the segments to elongate and push forward. Contraction of longitudinal muscles in segments behind a bulging region Lumbricus-A Representative "Oligochaete" pulls those segments fmward. Thus, segments move fo1ward Oligochaetes are found throughout the world in freshwater relative to the burrow as waves of muscle contraction move and terrestrial hahitats (see table 12.1). A few oligochaetes anteriorly on the worm (figure 12.16). are estuarine, and some are marine. Aquatic species live in Burrowing is the result of coelomic hydrostatic pressure shallow water, where they burrow in mud and debris. Terres­ being transmitted toward the prostomium. As an ea1thworm trial species live in soils with high organic content and rarely pushes its way through the soil, it uses expanded posterior 232 CHAPTER TWELVE

Prostomium Maintenance Functions Oligochaetes are scav­ engers and feed primarily on fallen and decaying vegetation, which they drag into their burrows at night. The digestive tract is similar to that described in section 12.2 (figure 12.17). The mouth leads to a muscular pha1ynx. In the ea1thworm, pha- 1yngeal muscles attach to the body wall. The pha1ynx acts as a pump for ingesting food. The mouth pushes against food, and the pha1ynx pumps the food into the esophagus. The esopha­ gus is narrow and tubular, and frequently expands to form a stomach, crop, or gizzard; the latter two are common in terres­ trial species. A crop is a thin-walled storage structure, and a giz­ zard is a muscular, cuticle-lined grinding structure. Calciferous glands are evaginations of the esophageal wall that rid the body Anus of excess calcium absorbed from food. They also help regulate FIGURE 12.15 the pH of body fluids. A dorsal fold of the lumenal epithelium Subclass Oligochaeta. External structures of the earthworm, called the typhlosole substantially increases the surface area of Lumbricus terrestris. the intestine (figure 12.18). Earthworm respirato1y and circulatory functions are as Longitudinal muscles described for polychaetes. Some segmental vessels expand contracted Circular muscles and may be contractile. In the earthworm, for example, (setae protruded) contracted expanded segmental vessels surrounding the esophagus pro­ (setae withdrawn) pel blood between dorsal and ventral blood vessels and ante­ \. riorly in the ventral vessel toward the mouth. Even though these are sometime.� c:allect "hearts," the m;iin propulsive structures are the dorsal and ventral vessels (seefigure 12.17). The ventral nerve cords and all ganglia of oligochaetes have undergone a high degree of fusion. Other aspects of nervous structure and function are essentially the same as those of annelids described in section 12.2.

Reproduction and Development All oligo­ chaetes are monoecious and exchange sperm during copula­ tion. One or two pairs of testes and one pair of ovaries are located on the anterior septum of ce1tain anterior segments. Rot!, thP �pp1·m rh1rN "nrl the nvirl11rN h'7VP rili'7tPrl fnnnPk ".lt their proximal ends to draw gametes into their respective tubes. Testes are closely associated with three pairs of seminal vesicles, which are sites for maturation and storage of sperm prior to their release. Seminal receptacles receive sperm during copulation. A pair of ve1y small ovisacs, associ­ ated with oviducts, are sites for the maturation and storage of ◄◄----Anterior eggs prior to egg release (figure 12.19). During copulation of Lumb1icus, two worms line up FIGURE 12.16 facing in opposite directions, with the ventral surfaces of their Earthworm Locomotion. Arrows designate activity in specific anterior ends in contact with each other. This orientation lines segments of the body, and broken lines indicate regions of up the clitellum of one worm with the genital segments of contact with the substrate. From: A LIFJ:iUF/1\WRf/71:.'/JllATES' © 1979 w. n R11ssefl-H111uer the other worm. A mucous sheath that the clitellum secretes envelops the anterior halves of both worms and holds the segments and protracted setae to anchor itself to its burrow worms in place. Some species also have penile structures wall. Any person pursuing fishing worms experiences the effec­ and genital setae that help maintain contact between worms. tiveness of this anchor when ttying to extract a worm from its In Lumbricus, the sperm duct releases sperm, which travel burrow. Contraction of circular muscles transforms the prosto­ along the external, ventral body wall in sperm grooves mium into a conical wedge, 1 mm in diameter at its tip. Con­ formed when special muscles contract. Muscular contractions traction of body-wall muscles generates coelomic pressure that along this groove help propel sperm toward the openings forces the prostomium through the soil. During burrowing, of the seminal receptacles. In other oligochaetes, copulation earthworms swallow considerable quantities of soil. results in the alignment of sperm duct and seminal receptacle Annelida: The Metameric Body Form 233

Calciferous glands Crop

Suprapharyngeal ganglion

Buccal cavity

Septum

Typhlosole Peristomium Testis nerve cord

nerve cord blood vessel FIGURE 12.17 Earthworm Structure. Lateral view of the internal structures in the anterior segments of an earthworm. A single complete septum is shown.

Longitudinal muscles �-- Dorsal blood vessel Ovary Muscular wall of intestine

Anterior

,i 10 9 ) l 14 13 .. 15

FIGURE 12.19 Earthworm Reproduction. Mating earthworms, showing arrangements of reproductive structures and the path sperm take during sperm exchange (shown by arrows).

Ventral nervecord ------' Subneural blood vessel _____. ------Gland cell and chitinous materials that encircle the clitellum. The clitel­ lum secretes a food reserve, albumen, into the cocoon, and the FIGURE 12.18 worm begins to back out of the cocoon. Eggs are deposited in Earthworm Cross Section. The nephrostomes shown here the cocoon as the cocoon passes the openings to the oviducts, would actually be associated with the next anterior segment. The and sperm are released as the cocoon passes the openings to ventral pair of setae on one side has been omitted to show the the seminal receptacles. Fertilization occurs in the cocoon, and nephridiopore opening of a nephridium. as the worm continues backing out, the ends of the cocoon are sealed, and the cocoon is deposited in moist soil. openings, and sperm transfer is direct. Copulation lasts 2 to Spiral cleavage is modified, and there are no larval 3 h, during which both worms give and receive sperm. forms. Hatching occurs in one to a few weeks, depending Following copulation, the clitellum forms a cocoon forthe on the species, when young worms emerge from one end of deposition of eggs and sperm. The cocoon consists of mucoid the cocoon. 234 CHAPTER TWELVE

Freshwater oligochaetes also reproduce asexually. Asexual coelomic compartments, the leech has a single hydrostatic reproduction involves transverse division of a worm, fol­ cavity and uses it in a looping type of locomotion. Figure 12.21 lowed by the regeneration of missing segments. describes the mechanics of this locomotion. Leeches also swim using undulations of the body. Glade Hirudinea Many leeches feed on body fluids or the entire bod­ ies of other invertebrates. Some feed on the blood of ver­ The clade Hirudinea (hi"ru-din' e-ah) (L. hirudin, leech) con­ tebrates, including human blood. Leeches are sometimes tains approximately 500 species of leeches (see table 12.1). called parasites; however, the association between a leech Most leeches are freshwater; others are marine or completely and its host i.� relatively hrief. Therefore, clescrihing leeches terrestrial. Leeches prey on small invertebrates or feed on the as predatory is probably more accurate. Leeches are also body fluids of vertebrates. not species specific, as are most parasites. (Leeches are, however, class specific. That is, a leech that preys on a tur­ Maintenance Functions Leeches lack parapodia tle may also prey on an alligator, but probably would not and head appendages. Setae are absent in most leeches. In a prey on a fish or a frog.) few species, setae occur only on anterior segments. Leeches The mouth (or proboscis pore) of a leech opens in the are dorsoventrally flattened and taper anteriorly. They have middle of the anterior sucker. In some leeches, the anterior 34 segments, but the segments are difficult to distinguish exter­ digestive tract is modified into a protrusible proboscis, lined nally because they have become secondarily divided. Several inside and outside by a cuticle. In others, the mouth is armed seconda1y divisions, called annuli, are in each true segment. with three chitinous jaws. While feeding, a leech attaches to Anterior and posterior segments are usually modified into suck­ its prey by the anterior sucker and either extends its probos­ ers (figure 12.20). cis into the prey or uses its jaws to slice through host tissues. Modifications of body-wall musculature and the coelom Salivary glands secrete an anticoagulant called hirudin that influence patterns of leech locomotion. The musculature of prevents blood from clotting. leeches is more complex than that of other annelids. A layer of oblique muscles is between the circular and longitudinal muscle layers. In addition, dorsoventral muscles are respon­ sible for the typical leech flattening. The leech coelom has lost its metameric partitioning. Septa are lost, and connective tissue has invaded the coelom, resulting in a series of inter­ connecting sinuses. (a) These modifications have resulted in altered patterns of locomotion. Rather than being able to utilize independent

Anterior sucker (b)

Salivary gland

(c)

Annuli

(d) Crop

Crop diverticula FIGURE 12.21 Leech Locomotion. (a b) Intestinal diverticulum and Attachment of the posterior sucker causes reflexive release of the anterior sucker, contraction Intestine of circular muscles, and relaxation of longitudinal muscles. This Anus------�--=-W.., muscular activity compresses fluids in the single hydrostatic compartment, and the leech extends. (c and d) Attachment of the Posterior sucker---.-. anterior sucker causes reflexive release of the posterior sucker, the relaxation of circular muscles, and the contraction of longitudinal FIGURE 12.20 muscles, causing body fluids to expand the diameter of the leech. Internal Structure of a Leech. Annuli subdivide each true The leech shortens, and the posterior sucker again attaches. From: '"A segment. Septa do not subdivide the coelom. LIFE OF INVERTHBRATES"© 1979 W. D. Russell-Hunter. Annelida: The Metameric Body Form 235

How Do We Know about Feeding of the Medicinal Leech Hirudo medicinRtlis?

he medicinal leech uses the probing response but none of feeding responses. Surgical removal both temperature and the other behaviors. A warmed of the lip area just dorsal to the chemical senses to detect artificialblood mixture contain- proboscis pore removed the feed­ preyT and initiate a feeding response. ing small molecular components ing responses. In control animals, A feeding response involves a of blood elicited all of the feeding surgery to other regions of the leech series of stereotyped behaviors behaviors. Eliminating either NaCl body did not interfere with feeding. that includes probing, attaching, or arginine (an amino acid) from Elliott, E. J. (1986). Chemosensory stimuli biting, and ingestion. Elliot (1986) the mixture prevented the last three in feeding behavior of the leech Hirudo found that a permeable bag filled responses. A warmed bag contain­ medicinalis, Journal of Comparative ° with water warmed to 38 C elicited ing NaCl and arginine initiated all Physiology 159(3): 391-401.

Behind the mouth is a muscular pha1ynx that pumps with the production of coelomic fluid. Chloragogen tissue body fluids of the prey into the leech. The esophagus follows proliferates through the body cavity of most leeches. the pha1ynx and leads to a large stomach with lateral cecae. Most leeches ingest large quantities of blood or other body Reproduction and Development All leeches fluids and gorge their stomachs and lateral cecae, increasing reproduce sexually and are monoecious. None are capable their body mass 2 to 10 times. After engorgement, a leech can of asexual reproduction or regeneration. They have a single tolerate periods of fasting that may last for months. The diges­ pair of ovaries and from four to many testes. Leeches have a tive tract ends in a sho1t intestine and anus (seefigure 12.20). clitellum that includes three body segments. The clitellum is Leeches exchange gases across the body wall. Some present only in the spring, when most leeches breed. leeches retain the basic annelid circulataty pattern, but in most Sperm transfer and egg deposition usually occur in the leeches, it is highly modified, and coelomic sinuses replace same manner as described for the ea1thworm. A penis assists vessels. Coelomic fluid has taken over the function of blood sperm transfer between individuals. A few leeches transfer and, except in two orders, respirato1y pigments are lacking. sperm by expelling a spermatophore from one leech into the The leech nervous system is similar to that of other integument of another, a form of hypodermic impregnation. annelids. The suprapharyngeal and subpharyngeal ganglia Special tissues within the integument connect to the ovaries by and the pharyngeal connectives all fuse into a ne1ve ring that sh01t ducts. Cocoons are deposited in the soil or are attached surrounds the pharynx. Ganglia at the posterior end of the to underwater objects. There are no la1val stages, and the off­ animal fuse in a similar way. spring are mature by the following spring. Most leeches have photoreceptor cells in pigment cups (2 to 10) along the dorsal surface of the anterior segments. SECTION REVIEW 12.4 Normally, leeches are negatively phototactic, but when they Members of the clade Clitellata include the earthworms, other are searching for food, the behavior of some leeches changes, oligochaetes, and leeches (clade Hirudinea). They lack para­ and they become positively phototactic, which increases the podia, have few or no setae, and possess a clitellum. Oligo­ likelihood of contacting prey that happen to pass by. chaetes use body-wall muscles in burrowing and crawling, Hirudo medicinalis, the medicinal leech, has a well devel­ feed as scavengers, have a closed circulato1y system, have oped temperature sense, which helps it to detect the higher a ventral ne1vous system, and use metanephridia for excre­ body temperature of its mammalian prey. Other leeches are tion. Reproduction involves mutual sperm exchange by mon­ attracted to extracts of prey tissues. oecious partners. Development is direct within cocoons. All leeches have senso1y cells with terminal bristles in Leeches have a body wall with seconda1y divisions called a row along the middle annulus of each segment. These sen­ annuli, complex musculature, and the coelom is not divided s01y cells, called sensory papillae, are of uncertain function by septa. Leeches are predators whose internal functions are but are taxonomically important. similar to those found in oligochaetes. Leeches have 10 to 17 pairs of metanephridia, one per segment in the middle segments of the body. Their metane­ What is a parasite (see chapters 6 and 8)? Why is it more phridia are highly modified and possess, in addition to the accurate to describe leeches as predators rather than nephrostome and tubule, a capsule believed to be involved parasites? 236 CHAPTER TWELVE

BASAL ANf\/f•,LIO GHOUPS

LEARNING OUTCOME 1. Describe the phylogenetic status and life styles of the Chaetopteridae and the sipunculans.

The last two annelid groups covered in this chapter have been phylogenetic enigmas. In one case, the Chaetopteridae, we have a group that generations of zoologists had consid­ ered to be a family within the "Polychaeta." In the other case, Sipuncula, we have a group of worms that had been given phylum status. As we will see in the next section, recent molecular evidence is causing reconsideration of both of these taxonomic assignments.

FIGURE 12.23 Chaetopteridae Sipunculans. Sipunculans are found throughout the world's Chaetopterus, the parchment worm, is found worldwide in oceans, where they live in mud, sand, or rock crevices. Themiste relatively shallow temperate and tropical marine habitats. It pyroides is shown here. It is found in the substrate of temperate oceans at depths of 0-36 m. is a permanent resident of its tough, parchment U-shaped tube that lies buried in sandy substrates or is attached to hard substrates (figure 12.22). Tubes can get as long as 80 cm, middle segments of the worm create water currents, which and worms are typically 15-20 cm. Both ends of the tube are flow anterior to posterior through the tube. Parapodia on the open and protrude from the substrate. The body of the worm 12th segment of the worm, called wings, form a mucous bag is divided into three regions. The anterior region of the worm used for trapping food particles suspended in the water flow­ has a shovel-like mouth and a series of segments with highly ing through the tube. The mucus, along with trapped food modified bristle-like parapodia. Modified parapodia in the particles, is rolled into a 3 mm ball and passed anteriorly toward the mouth by a dorsal ciliated groove. Reproduction involves external fertilization, development of planktonic Waler movement trochophore larvae, and settling of juvenile worms to the substrate. Chaetopterids are also bioluminescent. The chem­ istry behind this bioluminescence is poorly understood. Bio­ , luminescent chemicals are emitted with secreted mucus and I produce fleeting green flashes and a long-lasting blue glow. Parchmentllke The function of this bioluminescence is poorly understood. U,lbe Some researchers think it may help deter predators.

l 1 Sipuncula Mouth Sipunculans (peanut worms) (si-pun'ku-lah) (L. siphuncutus, small tube) consist of about 350 species of burrowing worms found in oceans throughout the world. These worms live in mud, sand, or any protected retreat. Their name is derived from their habit of retracting into a peanut-shape when dis­ turbed. The anterior portion of the body, the introvert, can be extended and a group of tentacles surrounding the mouth is used in feeding. Sipunculans range in size from 2 mm to 75 cm (figure 12.23). Like the echiruans, sipunculans lack segmentation and parapodia. Gametes are released through metanephridial tubules, and external fertilization and devel­ FIGURE 12.22 opment results in the formation of trochophore larvae. Cbaetopterus. Chaetopterus lives in its U-shaped, parchment tube. Water circulates through the tube by the action of modified parapodia, called "fans." The wing-like parapodia on the 12th SECTION REVIEW 12.5 segment secrete a mucous net that filters food from the circulating water. The food cup rolls mucus and filtered food into a ball that is Chaetopteridae is a family of annelids whose members live passed to the mouth. in U-shaped parchment tubes. Their bodies are divided into Annelida: The Metameric Body Form 237

three regions. Highly modified parapodia function in creat­ the group until the mid-1800s. Since that time, many taxonomic ing water currents and secreting mucus, which entraps food studies have attempted to so1t out relationships within the phy­ particles brought into their tubes with the circulating water. lum and to other phyla. These studies have resulted in radically External fertilization leads to the development of trochophore different, and sometimes conflicting, interpretations of annelid la1vae. Sipunculids burrow in mud and sand of marine habi­ phylogenetics. tats. They extend their introvert for feeding, and they lack As described earlier, recent molecular studies affirm the segmentation. Reproduction is by external fertilization, and monophyly of the Annelida. They place the Chaetopteridae development includes trochophore larvae. and Sipuncula near the base of the annelid phylogeny and outside of the two major annelid clades, Errantia and Sed­ In what ways are the Chaetopteridae and sipunculans entaria (figure 12.24). The inclusion of sipunculans as anne­ "unusual annelids?" What features of their biology lids is still controversial, but we have done so in this chapter are annelid-like? because of the strength of this molecular evidence. One of the objections to including sipunculans in Annelida is the absence of segmentation in the group. Neither 12.6 FURTHER PHYLOGENETIC the echiuran nor the sipunculans are segmented, and the segmentation of the siboglinids and Chaetopteridae is highly CONSIDERATIONS modified. If one assumes that segmentation is an ancestral characteristic of the Annelida, then it must have been inde­ LEARNING OUTCOME pendently lost or modified ve1y early in annelid evolution 1. Formulate a conversation between a modern taxonomist (Sipuncula and Chaetopteridae) and later in more derived and a taxonomist who worked 100 years ago as they groups (Echiura and Siboglinidae). compare their perceptions of annelid taxonomy. The Clitellata are believed to have evolved from a group of polychaetes that invaded freshwater. A few species Taxonomic relationships within the Annelida are the subject of of freshwater polychaetes remain today. This freshwater inva­ intense research. The original classification of the Annelida can sion required the ability to regulate the salt and water content be traced back to Jean Baptiste Lamarck (1809), who estab­ of body fluids. In addition, direct development inside of a lished the taxon. He recognized the similarities between the oli­ cocoon rather than as free-swimming larval stages promoted gochaetes and the polychaeters, but the leeches were left out of the invasion of terrestrial environments.

Annelida Errantia II Sedentaria �,, � 0rr, ,s; "11'" rffe rffe IS rffe �� "rr, ,[fr J' ,s<:i. ;:Ji '(f-� -� �0 -JJ :§' ,;:,'ll tb0 § '-0 s.;:; {$ .,,5 ,f' ,:! ,:,,0 -� �

FIGURE 12.24 Annelid Phylogeny. This molecular phylogeny shows one interpretation of the relationships among the annelids. It depicts the "Polychaeta" as a paraphyletic grouping and the Clitellata (Oligochaeta and Hirudinea) as well as the echiurans, siboglinids (pogonophorans), and sipunculans as groups nested within the polychaetes. The inclusion of the sipunculans within the Annelida is controversial, but supported by a growing body of evidence. 71:Jisphylogeny is based on Stmck, T. H. et at (2007), 'Annelid Phylogeny and tbe Statlls of Sipunrnla cmd Ecbium, "BMC Evolutionary Biology 7:57, http://www.biomedcentral.com/1471-2148- 7-57. 238 CHAPTER TWELVE

During the Cretaceous period, approximately 100 mya, this food resource. Some of the early freshwater sedentarians some sedentarian annelids invaded moist, terrestrial environ­ gave rise to leeches. Ancestral leeches then colonized marine i ments. This period saw the climax of the giant land reptiles, and terrestrial habitats from freshwater. Chapters 10 through 12 but more important, it was a time of proliferation of flower­ presented information on most of the better-known lophotro­ ing plants. The reliance of modern oligochaetes on deciduous chozoan phyla. Brief descriptions of three additional lesser­ vegetation can be traced back to their ancestors' exploitation of known lophotrochozoan phyla are presented in table 12.2.

TABLE 12.2 LESSER KNOWN LOPHOTROCHOZOANS

ENTOPROCTA

Examples Urnatellagracilis, Pedicellina cernua. Approximately 150 species. Description Entoprocta is a phylum of mostly sessile animals, ranging from 0.1 to 7 mm long. Mature individuals are goblet- shaped and attached by relatively long stalks. They have a crown of solid tentacles that bear cilia, which draw food particles toward the mouth. The mouth and anus Tentacles lie inside the crown. (Entoprotca means "anus inside.") Most entoprocts are colonial, and all but two species are marine. External fertilization is most common. Females lltill-.A....,._Rectum of other species retain ova in brood chambers where l>.-ll:l.....,_-Mouth they are fertilized and larvae develop. After hatching, the Stomach larvae swim for a short time, settle on a substrate, and Esophagus metamorphose to the adult.

Phylogenetic Fossils of entoproct.sare very rare and date from the Late (a) (b) Relationships Jurassic period. Some molecular phylogenies place the ento- procts in a clade with the ectoprocts and cycliophorans (see chapter 10).

PHORONIDA

Examples Phoronis architecha, Phoronopsis spp. Approximately Tentacles 20 species. Lophopore bearing Description Phoronids are vermiform, marine, and benthic tube mesostome dweliers. They use a lophophure in filler feeJiug. Their bodies (about 2 cm long) are divided into a flaplike epistome, Epistome a lophophore-bearing mesosome, and an elongate trunk Anus Nephridium (metasome). The gut is U-shaped and the anus is close to the mouth. All phoronids reproduce sexually. Phylogenetic There are scanty fossil records for Phoronida. Metastome Relationships Molecular phylogenies usually depict phoronids and Body wall brachiopods as sister groups within Lophotrochozoa Testis (see chapter 10). Intestine Ovary

MESOZOA

Examples Dicyema spp., Pseudicyemaspp., and Dicyemennea spp. Approximately 50 species. Vermiform embryos Description The mesozoans are enigmatic, minuscule, worm-like endoparasites of marine invertebrates. They are bilaterally symmetrical and lack tissues and organs. The body is only two cell layers thick in most places, and it consists of fewer than 50 cells. Reproduction is both sexual and asexual. Phylogenetic No fossil mesozoans are known. Molecular data and Reproductive cell Relationships contrasting morphologies suggest that "Mesozoa" may be polyphyletic-<:omposed of two phyla: Rhombozoa and Orthonectida. "Mesozoa" is now oftenapplied informally. Annelida: The Metameric Body Form 239

SECTlON REVIJ�W U? . fl Clitellata evolved from ancestral sedentarians that invaded fresh water. Annelida is monophyletic. Chaetopteridae and Sipuncula are basal annelids that lie outside of the Errantia and Sed­ Discuss the statement that segmentation is a defini­ entaria. Segmentation within the Annelida has been lost or tive, yet variable, characteristic of the Annelida. modified within basal and some derived annelid taxa. The

SUMMARY Fireworms feed on coral polyps and small crustaceans. Hol­ low setae are venomous, and their bright colors are an exam­ 12.1 Evolutionary Perspective ple of aposmatic coloration. The origin of the Annelida is largely unknown. Recent stud­ 12.4 Clade Sedentaria ies unite the annelids with molluscs and other phyla in the Sedentarians include a variety of marine tubeworms, the Lophotrochozoa. Recent molecular evidence divides the siboglinids, the echiruans, and the members of the clade Annelida into two major clades, Errantia and Sedentaria. Clitellata. Chaetopteridae and Sipuncula lie outside these clades. A diag­ Tubeworms construct tubes or live in burrows. They nostic characteristic of the annelids is metamerism. feed on organic matter in sea water, which they filter using Metamerism allows efficient utilization of separate coelomic cilia and mucus. Featherduster worms have a crown of compartments as a hydrostatic skeleton for support and move­ arm-like radioles that create water currents and trap food ment. Metamerism also lessens the impact of injmy and makes particles. tagmatization possible. Siboglinids live at great depths. They harbor symbiotic bacte­ 12. 2 Annelid Structure and Function ria that fix carbon dioxide into organic compounds. Most annelids possess parapodia with numerous setae. Locomo­ Echirurans are spoon worms. They live in marine burrows or tion involves the antagonism of longitudinal muscles on oppo­ rock crevices. They feed by sweeping organic material into site sides of the body, which creates undulatory waves along their spatula-shaped proboscis. the body wall and causes parapodia to act against the substrate. The clade Clitellata includes earthworms, other oligochaetes, Annelids may be predators, herbivores, scavengers, or filter and leeches (clade Hirudinea). They possess a clitellum used in feeders. cocoon formation. The nervous system of annelids usually consists of a pair of The earthworms and other "oligochaetes" are primarily fresh­ suprapharyngeal ganglia, subpharyngeal ganglia, and double water and terrestrial annelids. Oligochaetes possess few setae, ventral nerve cords that run the length of the worm. and they lack a head and parapodia. Annelids have a closed circulatory system. Respirat01y pig­ Earthworms are scavengers that feed on dead and decay­ ments dissolved in blood plasma carry oxygen. ing vegetation. Their digestive tract is tubular and straight, Annelids use either protonephridia or metanephridia in and it frequently has modifications for storing and grinding excretion. food and for increasing the surface area for secretion and Most annelids are dioecious, and gonads develop from coe­ absorption. lomic epithelium. Fertilization is usually external. Epitoky Earthworms are monoecious and exchange sperm during occurs in some polychaetes. copulation. Development of marine annelids usually results in a planktonic Members of the clade Hirudinea are the leeches. Complex trochophore la1va that buds off segments near the anus. Members arrangements of body-wall muscles and the loss of septa of the Clitellata are monoecious and have direct development. influence patterns of locomotion. 12.3 Clade Errantia Leeches are predat01y and feed on body fluids, the entire Members of the clade Errantia are mostly marine. They pos­ bodies of other invertebrates, and the blood of vertebrates. sess relatively long setae and well developed palps. Leeches are monoecious, and reproduction and development occur as in earthworms. Nereis, the clam worm, burrows in mud and sand substrates. It uses its proboscis and large jaws to feed on marine veg­ 12.5 Basal Annelid Groups etation and invertebrates. Reproduction occurs through Chaetopteridae are tl1e parchment worms. They live in swarming and external fertilization. Development includes a U-shaped parchment tubes and use highly modified para­ trochophore larval stage. podia in mucous-based filter feeding. Reproduction involves Clycera, the bloodworm, has hemoglobin-containing coe­ external fertilization and the development of trochophore lomocytes, burrows in mud and sand, and feeds on marine larvae. invertebrates. Reproduction occurs in a fashion similar to Sipunculans (the peanut worms) are marine burrowers that reproduction by Nereis. use an introvert in feeding. They are unsegmented. 240 CHAPTER TWELVE

12.6 Further Phylogenetic Considerations 4. Like many molluscs, annelid development usually involves Taxonomic studies affirm monophyly of the Annelida. Within a ____ larval stage. the Annelida, Chaetopteridae and Sipuncula are basal groups, a. veliger and Errantia and Sedentaria are the two major derived b. trochophore clades. Within the Sedentaria, members of the clade Clitellata C. glocidium invaded freshwater and terrestrial habitats. d. planula 5. After being released from the ____ of one earthworm, sperm is temporarily stored in the of a second earthworm. CONCEPT REVIEW QUESTIONS a. chloragogen tissue; nephridium 1. Current evidence indicates that b. seminal vesicles; seminal receptacles a. Annelida is a monophyletic group composed of two major c. testes; ovary clades, Errantia and Sedentaria. d. seminal vesicles; coelom b. Annelida is a paraphyletic group. c. Annelida is a monophyletic group, and its two clades (Polychaeta and Clitellata) are each clearly single-lineage ANALYSIS AND APPLICATION groups. QUESTIONS d. Annelida is a polyphyletic group, and the name should not be used as a phylum designation. 1. Distinguish between a protonephridium and a metanephrid­ ium. Name a group of annelids whose members may have 2. Which of the following statements is true regarding protonephridia. What other phylum have we studied whose metamerism? members also had protonephridia? Do you think that metane­ a. It arose only once in animal evolution. phridia would be more useful for an animal with an open or a b. It is foundonly in the Annelida and Chordata. closed circulato1y system? Explain. c. It permits a variety of locomotor and supp01tive functions 2. In what annelid groups are septa between coelomic compart­ not possible in nonmetameric animals. ments lost? What advantages does this loss give each group? d. Its main disadvantage is that it increases the likelihood that 3. What differences in nephridial function might you expect in injury will result in death of an animal. freshwater and marine annelids? 3. Which of the following statements about annelids 4. Relatively few annelids have invaded freshwater. Can you is true? think of a reasonable explanation for this? a. They have an open circulatory system. b. Their dorsal nerve cord begins anteriorly at suprapha1yn­ 11connect' geal ganglia. jzoOLOGY c. Most gas exchange occurs as a result of diffusion of gases Enhance your study of this chapter with study tools and practice across the body wall and parapodia. Some annelids have tests. Also ask your instructor about the resources available through parapodiai gills. Connect, including a media-rich eBook, interactive learning tools, d. Most adult annelids use protonephridia in excretion. and animations.